Abstract

Eggs of all animals contain mRNAs and proteins that are supplied to or deposited in the egg as it develops during oogenesis. These maternal gene products regulate all aspects of oocyte development, and an embryo fully relies on these maternal gene products for all aspects of its early development, including fertilization, transitions between meiotic and mitotic cell cycles, and activation of its own genome. Given the diverse processes required to produce a developmentally competent egg and embryo, it is not surprising that maternal gene products are not only essential for normal embryonic development but also for fertility. This review provides an overview of fundamental aspects of oocyte and early embryonic development and the interference and genetic approaches that have provided access to maternally regulated aspects of vertebrate development. Some of the pathways and molecules highlighted in this review, in particular, Bmps, Wnts, small GTPases, cytoskeletal components, and cell cycle regulators, are well known and are essential regulators of multiple aspects of animal development, including oogenesis, early embryogenesis, organogenesis, and reproductive fitness of the adult animal. Specific examples of developmental processes under maternal control and the essential proteins will be explored in each chapter, and where known conserved aspects or divergent roles for these maternal regulators of early vertebrate development will be discussed throughout this review.

Contents

• Introduction
  • Maternal-Effect Genes
  • Investigating Maternal Function
  • Targeting Maternal-Effect Genes
  • Genetics/Mutagenesis
  • Germline Replacement: Bypassing Essential Zygotic Functions
  • Morpholinos and Oligo RNaseH
  • RNAi
• Oogenesis: From Germline Stem Cells to Germline Cysts
• Oocyte Polarity and the Embryonic Axes: The Balbiani Body, an Ancient Oocyte Asymmetry
  • Molecular Control of Balbiani Body Development
  • Milton: Kinesin Adaptors and Mitochondrial Allocation
  • Bucky Ball: A Novel Regulator of Oocyte Asymmetry
  • MACF1/Magellan: A Role for Microtubule: Actin Cross-linkers in Balbiani Body Dynamics
• Preparing Developmentally Competent Eggs
  • Nuclear Maturation: Chromatin Modification
  • Maturation Cues: To Resume or Not to Resume Meiosis
  • Polarity Proteins Regulate the Cytoskeleton and Meiosis
  • Heat Shock Factor 1: Promoting Nuclear Maturation and Developmental Competence
  • Piwis: Silencing to Prevent Aneuploidy
  • mlh1/mps1: Mismatch Repair and Meiosis
  • Cytoplasmic Maturation: Clearing the Yolk in Fish
• Egg Activation
  • Zebrafish Egg Activation Mutants
• Blocking Polyspermy
  • Roles for Polarized Somatic Follicle Cell Types
  • Uchl1: A Role for Deubiquitination in Blocking Polyspermy
  • Basonuclin: A Zinc Finger Protein Involved in Developmental Competence and Limiting Sperm Entry
• Cleavage/Mitosis: Going Multicellular
  • Genetic Uncoupling of Karyokinesis and Cytokinesis in Zebrafish
  • Contributions of the Cytoskeleton to Cytokinesis and Karyokinesis
  • Cellular atoll/Sas6: Centrosome Duplication and Karyokinesis in Zebrafish
  • Pms2: A Role for Mismatch Repair in Preventing Aneuploidy
  • Geminin: Limiting Replication with Licensing Components
  • Microtubules and Motors: Regulating the Spindle and Polar Body
  • Tcl1: Contribution of a Cell Survival Factor to Embryonic Cleavages
• Maternal–Zygotic Transition
  • Providing Amino Acids via Autophagy
  • miRNAs: Silencing Maternal Messages
  • Zfp36l2: Zinc Finger-Mediated Clearance of Maternal Messages
  • A Clock Mechanism Regulates EGA in the Mouse
  • Promoting EGA /ZGA by Titration of Maternal Factors or Nucleocytoplasmic Ratio in Xenopus and Zebrafish
• Reprogramming: Epigenetic Modifications and Zygotic Genome Activation
  • DNMTs: Differential Methylation and Gene Expression
  • Zfp57: Establishing Maternal Marks and Maintaining Marks of Parental Origin
  • Dppa3/Stella/Pgc7: Preserving Maternal Marks
  • Modifying Histone and Switching from Maternal to Zygotic Histones
  • SLBP: Producing Enough Histone
  • Npm2: Regulating Nuclear Morphology and Unmasking mRNAs
  • HR6A: A Role for DNA Repair in Development Beyond the ZGA
  • SWI/SNF/TIFαα: Chromatin Remodeling to Activate Zygotic Gene Expression
  • Roles for Zinc Finger Proteins in Promoting Gene Expression
• Dorsal–Ventral Axis Formation before Zygotic Genome Activation in Zebrafish and Frogs
  • The Animal–Vegetal Oocyte Axis: Positioning and Translocation of Dorsal Determinants
  • Maternal Wnts and the Dorsal–Ventral Embryonic Axis-Signaling
  • Ichabod/β-Catenin Transcriptional Complex
  • Wnt Ligands
  • Receptors and Co-Receptors of Maternal Wnts
  • Cytoplasmic Factors Regulating Maternal β-Catenin
  • Intracellular Transducers of Wnt Signals
  • Maternal Wnts and the Dorsal Embryonic Axis-Translocation Machinery
  • Hecate: A Zebrafish Maternal-Effect Gene Required for Nuclear Accumulation of β-Catenin
  • Tokkaebe/Syntabulin: A Role in Dorsal Determinant Position and Release
  • Proper Egg Activation is Required for Dorsal Determinant Localization
• Maternal Tgf-β and the Dorsal–Ventral Embryonic Axis
  • TGFβ/BMP/Nodal: The Ligands and Cofactors
  • XPace4: Processing and Activating Maternal TGFβ
  • The Transcription Factors
  • Activators of Ventral Fate: A Role for Pluripotency Factors in Promoting Zygotic Expression of Transcription Factors that Regulate Ventral Fates
  • Ligands and Transducers of Ventral Fate
• Maternal Control After Zygotic Genome Activation
  • Inside versus Outside: Patterning the Mouse Blastocyst
  • Cdx2: A Maternal Contribution to Lineage Specification in the Mouse
  • Adhesion in Epithelia, Gastrulation, and Tissue Morphogenesis: G-protein-Coupled Receptors
  • Cadherin: Roles in Cohesion and Morphogenesis
  • Essential Regulators of Epiboly in Zebrafish
  • Regulating Epiboly in the Deep Cells
  • CREB: A Role for Transcription Factors During Gastrulation
  • Maternal Planar Cell Polarity Signaling in Gastrulation and Left–Right Patterning
  • Maternal Cilia Contribute to Zygote Signaling
  • Scribble: Regulating Migration of Gastrula Cells and Brachiomotor Neurons
• Compensation by Stable Maternal Proteins
  • Roles for Maternal Replication Complex and DNA Repair Components
  • Maternal Contributions to Segmentation and Somite Development
  • ALDH2: Maternal Roles for Retinoic Acid in Endoderm Development
  • GART and PAICS: Purine Synthesis and Pigmentation
• Maternal Contributions to Germline Establishment or Maintenance
• Perspective
• References