Oocyte Development

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Human-oocyte.jpg

Introduction

Historic drawing comparing the size of the mature human oocyte with a spermatozoa
Historic drawing comparing the size of the mature human oocyte with a spermatozoa

The oocyte (eggs, ova) is arrested at an early stage of the first {{meiosis))(first meiotic) division as a primary oocyte (primordial follicle) within the ovary. Following puberty, during each menstrual cycle, pituitary gonadotrophin stimulates completion of meiosis 1 the day before ovulation. Early oocytes are also classified as immature (germinal vesicle (GV) or metaphase I (MI) stage). The breakdown of the germinal vesicle indicates a resumption of meiosis and the extrusion of the first polar body (1 PB) indicates completion of the first meiotic division in human oocytes.

The released oocyte is surrounded by a thick specialised extracellular matrix, the zona pellucida, that in turn is covered in layers of cells, the granulosa layer.


In an adult human female, the development of a primordial follicle containing an oocyte to a preovulatory follicle takes in excess of 120 days.


Genital Links: genital | Lecture - Medicine | Lecture - Science | Lecture Movie | Medicine - Practical | primordial germ cell | meiosis | Female | X | ovary | oocyte | uterus | vagina | reproductive cycles | menstrual cycle | Male | Y | testis | spermatozoa | penis | prostate | endocrine gonad‎ | Genital Movies | genital abnormalities | Assisted Reproductive Technology | puberty | Category:Genital
Historic Embryology - Genital 
1901 Urinogenital Tract | 1902 The Uro-Genital System | 1904 Ovary and Testis | 1904 Leydig Cells | 1904 Hymen | 1905 Testis vascular | 1909 Prostate | 1912 Prostate | 1912 Urinogenital Organ Development | 1914 External Genitalia | 1914 Female | 1915 Cowper’s and Bartholin’s Glands | 1920 Wolffian tubules | 1921 Urogenital Development | 1921 External Genital | 1927 Female Foetus 15 cm | 1932 Postnatal Ovary | 1935 Prepuce | 1935 Wolffian Duct | 1942 Sex Cords | 1943 Testes Descent | 1953 Germ Cells | Historic Embryology Papers | Historic Disclaimer
Historic Embryology - Oocyte  
1919 Human Ovum | 1921 The Ovum | 1929 Oocyte Size

Some Recent Findings

  • Oocyte-specific deletion of Gsα induces oxidative stress and deteriorates oocyte quality in mice[1] "The stimulatory heterotrimeric Gs protein alpha subunit (Gsα) is a ubiquitous guanine nucleotide-binding protein that regulates the intracellular cAMP signaling pathway and consequently participates in a wide range of biological events. In the reproductive system, despite Gsα being associated with oocyte meiotic arrest in vitro, the exact role of Gsα in female fertility in vivo remains largely unknown. Here, we generated oocyte-specific Gsα knockout mice by using the Cre/LoxP system. We observed that the deletion of Gsα caused complete female infertility. Exclusion of post-implantation abnormalities, oogenesis, fertilization, and early embryo development was subsequently monitored; meiosis in Gsα-deficient oocytes precociously resumed in only 43% of antral follicles from mutant mice, indicating that alteration of meiotic pause was not the key factor in infertility. Ovulation process and number were normal, but the rate of morphological abnormal oocytes was apparently increased; spindle organization, fertilization, and early embryo development were impaired. Furthermore, the level of ROS (reactive oxygen species) and the mitochondrial aggregation increased, and antioxidant glutathione (GSH) content, ATP level, mtDNA copy number, and mitochondrial membrane potential decreased in Gsα-deficient oocytes. GV oocytes from mutant mice showed early-stage apoptosis. Meanwhile, the Gsα knockout-induced decline in oocyte quality and low developmental potential was partially rescued by antioxidant supplementation."
  • Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice[2] "MTOR (mechanistic target of rapamycin) is a widely recognized integrator of signals and pathways key for cellular metabolism, proliferation, and differentiation. Here we show that conditional knockout (cKO) of Mtor in either primordial or growing oocytes caused infertility but differentially affected oocyte quality, granulosa cell fate, and follicular development. ...Therefore, MTOR-dependent pathways in primordial or growing oocytes differentially affected downstream processes including follicular development, sex-specific identity of early granulosa cells, maintenance of oocyte genome integrity, oocyte gene expression, meiosis, and preimplantation developmental competence."
  • Complete in vitro oogenesis: retrospects and prospects[3] "In reality the vast majority of oocytes formed from primordial germ cells (PGCs) will undergo apoptosis, or other forms of cell death. Removal occurs during germ cell cyst breakdown and the establishment of the primordial follicle (PF) pool, during the long dormancy at the PF stage, or through follicular atresia prior to reaching the ovulatory stage. A way to solve this limitation could be to produce large numbers of oocytes, in vitro, from stem cells. However, to recapitulate mammalian oogenesis and produce fertilizable oocytes in vitro is a complex process involving several different cell types, precise follicular cell-oocyte reciprocal interactions, a variety of nutrients and combinations of cytokines, and precise growth factors and hormones depending on the developmental stage. In 2016, two papers published by Morohaku et al. and Hikabe et al. reported in vitro procedures that appear to reproduce efficiently these conditions allowing for the production, completely in a dish, of a relatively large number of oocytes that are fertilizable and capable of giving rise to viable offspring in the mouse. The present article offers a critical overview of these results as well as other previous work performed mainly in mouse attempting to reproduce oogenesis completely in vitro and considers some perspectives for the potential to adapt the methods to produce functional human oocytes."
  • A stereological study on organelle distribution in human oocytes at prophase I[4] "The ultrastructural analysis of human oocytes at different maturation stages has only been descriptive. The aim of this study was to use a stereological approach to quantify the distribution of organelles in oocytes at prophase I (GV). Seven immature GV oocytes were processed for transmission electron microscopy and a classical manual stereological technique based on point-counting with an adequate stereological grid was used. The Kruskal-Wallis test and Mann-Whitney U-test with Bonferroni correction were used to compare the means of the relative volumes occupied by organelles in oocyte regions: cortex (C), subcortex (SC) and inner cytoplasm (IC). Here we first describe in GV oocytes very large vesicles of the smooth endoplasmic reticulum (SER), vesicles containing zona pellucida-like materials and coated vesicles. The most abundant organelles were the very large vesicles of the SER (6.9%), mitochondria (6.3%) and other SER vesicles (6.1%). Significant differences in organelle distribution were observed between ooplasm regions: cortical vesicles (C: 1.3% versus SC: 0.1%, IC: 0.1%, P = 0.001) and medium-sized vesicles containing zona pellucida-like materials (C: 0.2% versus SC: 0.02%, IC: 0%, P = 0.004) were mostly observed at the oocyte cortex, whereas mitochondria (C: 3.6% versus SC: 6.0%, IC: 7.2%, P = 0.005) were preferentially located in the subcortex and inner cytoplasm, and SER very large vesicles (IC: 10.1% versus C: 0.9%, SC: 1.67%, P = 0.001) in the oocyte inner cytoplasm." Prophase I | meiosis
More recent papers  
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Search term: Oocyte Development

Yan Bai, Chengdong Liu, Jianfeng Zhou, Xiaozhi Rong, Hongying Wang Molecular, functional, and gene expression analysis of zebrafish Ror1 receptor. Fish Physiol. Biochem.: 2018; PubMed 30242697

Christine Wrenzycki Gene expression analysis and in vitro production procedures for bovine preimplantation embryos: Past highlights, present concepts and future prospects. Reprod. Domest. Anim.: 2018, 53 Suppl 2;14-19 PubMed 30238652

Marketa Koncicka, Anna Tetkova, Denisa Jansova, Edgar Del Llano, Lenka Gahurova, Jana Kracmarova, Sarka Prokesova, Tomas Masek, Martin Pospisek, Alexander W Bruce, Michal Kubelka, Andrej Susor Increased Expression of Maturation Promoting Factor Components Speeds Up Meiosis in Oocytes from Aged Females. Int J Mol Sci: 2018, 19(9); PubMed 30235877

Yan Guo, Ary A Hoffmann, Xiao-Qin Xu, Pei-Wen Mo, Hai-Jian Huang, Jun-Tao Gong, Jia-Fei Ju, Xiao-Yue Hong ##Title## Front Microbiol: 2018, 9;2016 PubMed 30233514

Liyuan Li, Zhao Wang Ovarian Aging and Osteoporosis. Adv. Exp. Med. Biol.: 2018, 1086;199-215 PubMed 30232761

Older papers  
  • Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women[5] "Germline stem cells that produce oocytes in vitro and fertilization-competent eggs in vivo have been identified in and isolated from adult mouse ovaries. Here we describe and validate a fluorescence-activated cell sorting-based protocol that can be used with adult mouse ovaries and human ovarian cortical tissue to purify rare mitotically active cells that have a gene expression profile that is consistent with primitive germ cells. Once established in vitro, these cells can be expanded for months and can spontaneously generate 35- to 50-μm oocytes, as determined by morphology, gene expression and haploid (1n) status. Injection of the human germline cells, engineered to stably express GFP, into human ovarian cortical biopsies leads to formation of follicles containing GFP-positive oocytes 1-2 weeks after xenotransplantation into immunodeficient female mice. Thus, ovaries of reproductive-age women, similar to adult mice, possess rare mitotically active germ cells that can be propagated in vitro as well as generate oocytes in vitro and in vivo." (these cells described as oogonial stem cells (OSCs), are very rare—only about 1 out of 10,000 ovarian cells)

Movies

Oocyte Meiosis 01 icon.jpg
 ‎‎Oocyte Meiosis
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Rabbit-ovulation.jpg
 ‎‎Ovulation
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Follicle 001 icon.jpg
 ‎‎Ovulation
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Bovine uterine tube oocyte transport 1.jpg
 ‎‎Oocyte Transport
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Fertilization 002 icon.jpg
 ‎‎Fertilization
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Fertilization 001 icon.jpg
 ‎‎Mouse Fertilisation
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Pronuclear fusion 001 icon.jpg
 ‎‎Pronuclear Fusion
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DNA bead-induced ectopic polar body-icon.jpg
 ‎‎Ectopic Polar Body
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Movies

Oogenesis

Infant ovary.jpg

A human infant ovary histology, showing the large number of oocytes occupying the ovary cortical region. Compare this with a mature ovary and note the absence of any follicle development in the infant. These early oocytes remain at the diplotene stage of the meiosis I during development from fetal life and postnatal childhood, until puberty when the lutenizing hormone (LH) surges stimulate the resumption of meiosis.

Primordial Follicle

HertigAdams1967 fig04.jpg

Electron Micrograph of a human oocyte in a primordial follicle. Most of the organelles are concentrated in one pole of the oocyte.[6]

Secondary Follicle

Secondary follicle with oocyte]

Secondary follicle with oocyte


The graph below shows the changes in human germ cell numbers in the ovary with age, peaking at about 7 million (occuring in early fetal development) and then decreasing by apopotic cell death. At puberty there remain only about 400,000 and only about 10% of these will be released through reproductive life. (More? Menstrual Cycle)

Human ovary non-growing follicle model

Human ovary non-growing follicle model[7]

Links: Ovary Development | Assisted Reproductive Technology

Oocyte Growth

Ovary oocyte size graph

Graph shows species comparison in oocyte size growth (diameter) at different stages of follicle development.[8] (See also Follicle size graph)

Human Follicle Classification
Follicle class Alternate nomenclature Type Number of Cells Size (diameter µm)
Primordial small 1, 2, 3 25 less than 50
Primary preantral 4
5
26 - 100
101 - 300
up to 200
Secondary small antral
large antral
6
7
3001 - 500
501 - 1000
500
1000 - 6000
Preovulatory Graafian 8 greater than 1000 greater than 6000
  Links: Ovary Development | Oocyte Development

Meiosis

Human Oocyte metaphase of meiosis 2
Human Oocyte metaphase of meiosis 2

In females, the total number of eggs ever to be produced are present in the newborn female initially arrested at the diplotene stage of the meiosis I from fetal life through childhood until puberty, when the lutenizing hormone (LH) surges stimulate the resumption of meiosis.

  1. All eggs are arrested at an early stage (prophase I) of the first meiotic division as a primary oocyte (primordial follicle). Following purberty, during each menstrual cycle, pituitary gonadotrophin stimulates completion of meiosis 1 the day before ovulation.
  2. In meiosis 1, a diploid cell becomes 2 haploid (23 chromosomes) daughter cells, each chromosome has two chromatids. One cell becomes the secondary oocyte the other cell forms the first polar body.
  3. The secondary oocyte then commences meiosis 2 which arrests at metaphase and will not continue without fertilization.
  4. At fertilization meiosis 2 completes, forming a second polar body. Note that the first polar body may also undergo this process forming a third polar body.

Female gametogenesis


Links: meiosis

Polar Body

Human oocyte at metaphase II showing polar body at top

The polar body is a small cytoplasmic exclusion body formed to enclose the excess DNA formed during the oocyte (egg) meiosis and following sperm fertilization. The breakdown of the germinal vesicle indicates a resumption of meiosis and the extrusion of the first polar body (1 PB) indicates completion of the first meiotic division in human oocytes.


There are 2-3 polar bodies derived from the oocyte present in the zygote, the number is dependent upon whether polar body 1 (the first polar body formed during meiosis 1) divides during meiosis 2. This exclusion body contains the excess DNA from the reductive division (the second and third polar bodies are formed from meiosis 2 at fertilization). These polar bodies do not contribute to the future genetic complement of the zygote, embryo or fetus.

Recent research in some species suggest that the space formed by the peripheral polar body (between the oocyte and the zona pellucia) can influence the site of spermatozoa fertilization.

Polar Body Extrusion Model

The following cartoon model from mouse oocyte study of polar body extrusion, involving cortical cap protrusion and spindle midzone-induced membrane furrowing.[9]

Polar body extrusion model
(A) Chromosomes induce formation of a cortical actomyosin cap/ring prior to polar body extrusion. (B) Egg activation induces the cortical cap protrusion. (C) The anaphase spindle midzone induces unilateral furrowing. (D) Spindle rotation. (E) Spindle midzone induces bilateral furrowing and abscission of polar body.
The squared region of the cortical cap/ring is shown on the top, an actin cap (red) surrounded by a myosin II ring (green).

Assisted reproductive techniques involving intracytoplasmic sperm injection (ICSI) have looked at the "quality" of the polar body and found that the morphology is related to mature oocyte viability and has the potential to predict oocyte fertilization rates and pregnancy achievement.[10][11]


Links: Meiosis

Calcium Release

Oocyte calcium ion (Ca2+) release occurs after spermatozoa fusion and is part of the reactivation of meiosis (arrested at metaphase II) and the primary block to polyspermy. Earlier in oocyte meiosis, between prophase I (germinal vesicle stage) and MII, this release mechanism is developed within the cell.

Oocyte cytoplasmic changes include:

  1. endoplasmatic reticulum reorganization.
  2. IP3 receptor increase in both number and sensitivity.
  3. increase in calcium ion concentration.

Cortical Granules

Human oocyte (MII) showing cortical granules
Human oocyte (MII) showing cortical granules (green)
Mouse oocyte cortical granules
Mouse oocyte cortical granules (red)

The release of cortical granules by exocytosis, the "cortical reaction", occurs following spermatozoa fertilisation and is the main block to polyspermy by modifying the zone pellucida. These granules develop from the golgi apparatus initially forming smaller vesicles that coalesce to form mature membrane bound cortical granules (0.2 to 0.6 microns in diameter) located in the cortex of unfertilized oocytes. In mammals, cortical granule production in the developing follicular oocyte is an ongoing and continuous process, with newly synthesized granules translocating to the cortex until the time of ovulation.

Cortical granules:

  • vary in time of initial development between species.
    • primordial follicle stage - rat and mouse.
    • primary follicle stage - human, monkey, hamsters, and rabbit.
  • vary in type formed in the same species.
  • migration requires the microfilaments of the cell cytoskeleton.
  • are evenly distributed in the cortex of unfertilised oocytes.
  • contain carbohydrates, proteinases, ovoperoxidase, calreticulin, N-acetylglucosaminidase


Ovastacin

  • oocyte-specific member of the astacin family
  • mouse cortical granule protease (metalloendoproteases)
  • cleaves zona pellucida ZP2
  • female mice lacking ovastacin do not cleave ZP2 after fertilisation[12]


Oocyte-Follicle Cell Interaction

The oocyte and the surrounding granulosa cells have a complex paracrine interactions during follicle growth and development. Oocyte maturation has been shown to depend on secretory products of both the granulosa and cumulus cells.

Oocyte Factors

  • promotes granulosa cell proliferation in preantral and antral follicles (GDF-9, BMP15)
  • cumulus expansion and granulosa cell differentiation are dependent upon oocyte-derived factors
  • BMP15 inhibits FSH-stimulated progesterone production

Oocyte Different Species

1929 Hartman - Species Oocyte Sizes  
Animal Most probable size of egg (μm) Jenkinson's Table
Monotremata
Platypus 1.5 mm
Echidna 3 .0 mm
Marsupialia
Dasyurus 240 280
Didelphis 140-160 130
Edentata
Armadillo 80
Cetacea
Whales 140
Insectivora
Mole (Talpa) 12.5 90
Hedgehog (Erinaceus) 100 60
Rodentia
Mouse 70-75 60
Rat 70-75
Guinea pig 75-85 80
Lagomorpha
Rabbit 120-130 150
Carnivora
Dog 135-145 180
Cat 120-130
Ferret 120
Ungulata
Horse 135
Sheep 120 150
Goat 140
Pig 120-140
Cheiroptera
Bat 95-105
Lemurs
Tarsius 90
Primates
Gibbon 110-110
M. rhesus 110-120
Gorilla 130-140
Man 130-140
Jenkinson Table - JW. Jenkinson Vertebrate Embryology. (1913) Oxford. (Gives a table of egg sizes.)

Table 8 Reference: Hartman CG. How Large is the Mammalian Egg?: A Review. (1929) Quart. Rev. Biol., 4(3): 373-388.

Balbini Body

Mouse oocyte balbini body EM
Mouse oocyte balbini body EM[13]

The Balbiani body (Balbiani vitelline body; mitochondrial cloud) is a large organelle aggregate found in developing oocytes of many species.[14], including human.[15][16] Located asymmetrically beside the nucleus and is composed of: endoplasmic reticulum, mitochondria, Golgi, and proteins. In the human fetal ovary oocyte development, the RNA binding protein VASA protein is expressed in primordial follicles has been shown to colocalise to Balbiani's vitelline space.[17] Note VASA expression is not detectable in the adult ovary.

Balbini Body History  
Prof. Édouard-Gérard Balbiani (1823–1899)
  • 1864 - Balbiani first described this structure in oocytes of spiders and myriapods.
  • 1887 - Henneguy (Balbiani‘s student) first named the structure “Balbiani’s vesicle”.
  • 1893 - Balbiani summarized his earlier observations. Henneguy now names this structure the “yolk body of Balbiani”.
  • 1923 - Van der Stricht identified this "central vitelline" or "Balbiani body" separately from the surrounding. vitellogenic or mitochondrial bed.

For more information see Hertig's 1968 presentation.[15]

References

Balbiani EG. Recherches sur les phénomenes sexuels des Infusoires. (1864) J. de la Physiol. 4: 102-130.

Balbiani EG. Recherches sur les phénomenes sexuels des Infusoires. (1864) J. de la Physiol. 4: 194- 220.

Balbiani EG. Centrosome et “Dotterkern.” (1893) J. Anat. Physiol. 29: 145-180.

van der Stricht O. Comparative study of mammalian ovum at the different periods of ovogenesis, according to the work of the histology and embryology laboratory of the University of Ghent. Etude comparée des ovules des mammiferes aux diflerentes periods de Yovogenese, d’aprés les travaux du laboratoire d’histo1ogie et d’embryologie de l’université de Gand. (1923) Arch. Biol., 33: 229-300.

Edouard Gerard Balbiani.jpg


Édouard-Gérard Balbiani (1823–1899)


Oocyte Metabolism

SIRT1 cell distribution
SIRT1 cell distribution.[18]

In the mouse, the secondary follicle stage through to large antral follicle stage the oocyte has a highly oxidative metabolism. In contrast, the surrounding surrounding granulosa and cumulus cells are highly glycolytic. In this second group, the cumulus cells are found to be more glycolytic than the granulosa cells.[19]

  • oxidative metabolism - requires oxygen (aerobic) to make energy from carbohydrates (sugars) into pyruvate that passes into the mitochondria where it is fully oxidised by oxygen into carbon dioxide. Also called aerobic metabolism, aerobic respiration, and cell respiration.
  • glycolytic metabolism - requires no oxygen (anaerobic) to make energy from carbohydrates (sugars) into pyruvate that is reduced by adenine dinucleotide hydride (NADH).


In the cat oocyte, in pre-antral oocytes mitochondria have a homogeneous distribution throughout the cytoplasm. In the antral stage they have relocated to a mainly pericortical distribution.[20]


Links: OMIM SIRT1

Oocyte Protein Expression

Mouse- germinal vesicle oocyte protein expression

Mouse- MII oocyte protein expression

The table above shows the pattern of protein expression (as percentages of total) in the mouse germinal vesicle and MII oocyte according to 14 molecular function categories.[21]

Links: Germinal vesicle oocyte protein expression | MII oocyte protein expression | Zygote Protein Expression | Mouse Development | Oocyte Development | Zygote

Oocyte Telomerase Reverse Transcriptase

There is a redistribution of the enzyme that regulates telomere length during oocyte development. The following oocyte images are from a recent study of sheep in vitro follicle development.[22]

Sheep oocyte image Sheep oocyte image
preantral early antral
Sheep oocyte image Sheep oocyte image
early antral preovulatory follicle
  • TERT - Red (Cy3-conjugated secondary antibody) (telomerase reverse transcriptase, TERT)
  • DNA - Green (SYBR Green 14/I)


Sheep Oocyte TERT: preantral | early antral | early antral | preovulatory follicle | Oocyte Development | Sheep Development

Abnormalities

Trisomy 21 female karyotype

Meiotic non-disjunction resulting in aneuploidy, most are embryonic lethal and not seen. The potential for genetic abnormalities increase with maternal age.

Autosomal chromosome aneuploidy Sex chromosome aneuploidy
  • monosomy X - Turner's Syndrome
  • trisomy X - Triple-X syndrome
  • 47 XXY - Klinefelter's Syndrome


Links: Trisomy 21 | Abnormal Development - Genetic | Genital System - Abnormalities

Additional Images

Historic Images

Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Hamilton WJ. Phases of maturation and fertilization in human ova. (1944) J Anat. 78: 1-4.

Pincus G. and Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro. (1935) J Exp Med. 62(5): 665-75. PMID 19870440

References

  1. Xie Y, Wu B, Jin Y, Zhang A, Sun X, Zhang X, Gao X, Dong R, Li H & Gao J. (2018). Oocyte-specific deletion of Gsα induces oxidative stress and deteriorates oocyte quality in mice. Exp. Cell Res. , , . PMID: 30026030 DOI.
  2. Guo J, Zhang T, Guo Y, Sun T, Li H, Zhang X, Yin H, Cao G, Yin Y, Wang H, Shi L, Guo X, Sha J, Eppig JJ & Su YQ. (2018). Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice. Proc. Natl. Acad. Sci. U.S.A. , , . PMID: 29784807 DOI.
  3. Wang JJ, Ge W, Liu JC, Klinger FG, Dyce PW, De Felici M & Shen W. (2017). Complete in vitro oogenesis: retrospects and prospects. Cell Death Differ. , 24, 1845-1852. PMID: 28841213 DOI.
  4. Pires-Luís AS, Rocha E, Bartosch C, Oliveira E, Silva J, Barros A, Sá R & Sousa M. (2016). A stereological study on organelle distribution in human oocytes at prophase I. Zygote , 24, 346-54. PMID: 26170179 DOI.
  5. White YA, Woods DC, Takai Y, Ishihara O, Seki H & Tilly JL. (2012). Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat. Med. , 18, 413-21. PMID: 22366948 DOI.
  6. Hertig AT. and Adams EC. Studies on the human oocyte and its follicle. I. Ultrastructural and histochemical observations on the primordial follicle stage. (1967) J Cell Biol. 34(2):647-75. PMID 4292010
  7. Wallace WH & Kelsey TW. (2010). Human ovarian reserve from conception to the menopause. PLoS ONE , 5, e8772. PMID: 20111701 DOI.
  8. Griffin J, Emery BR, Huang I, Peterson CM & Carrell DT. (2006). Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J. Exp. Clin. Assist. Reprod. , 3, 2. PMID: 16509981 DOI.
  9. Wang Q, Racowsky C & Deng M. (2011). Mechanism of the chromosome-induced polar body extrusion in mouse eggs. Cell Div , 6, 17. PMID: 21867530 DOI.
  10. Ebner T, Yaman C, Moser M, Sommergruber M, Feichtinger O & Tews G. (2000). Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum. Reprod. , 15, 427-30. PMID: 10655316
  11. Younis JS, Radin O, Izhaki I & Ben-Ami M. (2009). Does first polar body morphology predict oocyte performance during ICSI treatment?. J. Assist. Reprod. Genet. , 26, 561-7. PMID: 19960239 DOI.
  12. Burkart AD, Xiong B, Baibakov B, Jiménez-Movilla M & Dean J. (2012). Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J. Cell Biol. , 197, 37-44. PMID: 22472438 DOI.
  13. Pepling ME, Wilhelm JE, O'Hara AL, Gephardt GW & Spradling AC. (2007). Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc. Natl. Acad. Sci. U.S.A. , 104, 187-92. PMID: 17189423 DOI.
  14. Cox RT & Spradling AC. (2003). A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development , 130, 1579-90. PMID: 12620983
  15. 15.0 15.1 Hertig AT. (1968). The primary human oocyte: some observations on the fine structure of Balbiani's vitelline body and the origin of the annulate lamellae. Am. J. Anat. , 122, 107-37. PMID: 5654499 DOI.
  16. Wessel GM. (2012). Clouded by terminology: Edouard-Gérard Balbiani and the mitochondrial cloud. Mol. Reprod. Dev. , 79, Fm i. PMID: 22987576 DOI.
  17. Albamonte MI, Albamonte MS, Stella I, Zuccardi L & Vitullo AD. (2013). The infant and pubertal human ovary: Balbiani's body-associated VASA expression, immunohistochemical detection of apoptosis-related BCL2 and BAX proteins, and DNA fragmentation. Hum. Reprod. , 28, 698-706. PMID: 23315064 DOI.
  18. Aguilar-Arnal L, Ranjit S, Stringari C, Orozco-Solis R, Gratton E & Sassone-Corsi P. (2016). Spatial dynamics of SIRT1 and the subnuclear distribution of NADH species. Proc. Natl. Acad. Sci. U.S.A. , , . PMID: 27791113 DOI.
  19. Cinco R, Digman MA, Gratton E & Luderer U. (2016). Spatial Characterization of Bioenergetics and Metabolism of Primordial to Preovulatory Follicles in Whole Ex Vivo Murine Ovary. Biol. Reprod. , 95, 129. PMID: 27683265 DOI.
  20. Songsasen N, Henson LH, Tipkantha W, Thongkittidilok C, Henson JH, Chatdarong K & Comizzoli P. (2017). Dynamic changes in mitochondrial DNA, distribution and activity within cat oocytes during folliculogenesis. Reprod. Domest. Anim. , 52 Suppl 2, 71-76. PMID: 28111812 DOI.
  21. Wang S, Kou Z, Jing Z, Zhang Y, Guo X, Dong M, Wilmut I & Gao S. (2010). Proteome of mouse oocytes at different developmental stages. Proc. Natl. Acad. Sci. U.S.A. , 107, 17639-44. PMID: 20876089 DOI.
  22. Barboni B, Russo V, Cecconi S, Curini V, Colosimo A, Garofalo ML, Capacchietti G, Di Giacinto O & Mattioli M. (2011). In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation. PLoS ONE , 6, e27550. PMID: 22132111 DOI.


Reviews

Li R & Albertini DF. (2013). The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell Biol. , 14, 141-52. PMID: 23429793 DOI.

Sánchez F & Smitz J. (2012). Molecular control of oogenesis. Biochim. Biophys. Acta , 1822, 1896-912. PMID: 22634430 DOI.

Liu M. (2011). The biology and dynamics of mammalian cortical granules. Reprod. Biol. Endocrinol. , 9, 149. PMID: 22088197 DOI.

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Oocyte Development

Note there are additional specific term glossaries available listed at bottom of this table.

  • antral follicle - (secondary) the stage following preantral in the decription of the sequence ovarian follicle development.
  • antrum - (L. a cave), cavity; a nearly-closed cavity or bulge. In the ovary this refers to the follicular fluid-filled space within the follicle.
  • atretic follicle - An ovarian follicle that fails to mature and degenerates. Also called "atresia" refering to the process of degeneration of the ovarian follicle. This process can occur at any stage of follicle development (folliculogenesis).
  • clomiphene citrate - drug taken orally to promote the process of follicle/egg maturation.
  • COCs - cumulus-oocyte complexes, term used in Assisted Reproductive Technology to describe the ovulated Graafian follicle consisting of the oocyte surrounded by a packed layers of cumulus cells.
  • corona radiata - Layer of follicle cells of cumulus oophorus remaining directly attached to zona pellucida of the oocyte. These cells communicate with the oocyte through the zone pellucida, also called granulosa cells.
  • corpus albicans - (L. corpus = body, L. albicans = whitish); a degenerating corpus luteum in ovary.
  • corpus luteum - (L. corpus = body, L. luteum = yellow) The remains of the ovulating ovarian follicle after ovulation, that acts as the initial endocrine organ supporting pregnancy and preventing menstruation (loss of the endometrial lining). de Graaf first observed it in the ovary of a cow as a yellow structure.
  • cortical - (L. corticalis) at the outside (like the bark of a tree), usually combined with medulla meaning the core.
  • cumulus oophorus - (L. cumulus = a little mound G. oon = egg + phorus = bearing); part of the wall of an ovarian follicle surrounding and carrying the ovum (oocyte).
  • follicle - (L. folliculus = little bag,dim. of L. follis). A structure which develops in the ovary and contains a developing egg (oocyte).
  • follicle stimulating hormone - (FSH, gonadotropin) A glycoprotein hormone secreted by anterior pituitary (adenohypophysis gonadotrophs, a subgroup of basophilic cells) and acts on gametogenesis and other systems in both males and females. Females, FSH acts on the ovary to stimulate follicle development. Males, acts on the testis Sertoli cells to increase androgen-binding protein (ABP) that binds androgens and has a role in spermatogenesis. pituitary
  • follicular fluid - the fluid found in the antrum of a secondary follicle. Secreted by cells in the wall of the follicle. This fluid is released along with the oocyte at ovulation.
  • germinal epithelium - cellular component covering surface of ovary, it is continuous with mesothelium covering mesovarium. Note that it is a historical misnomer, as it is not the actual site of germ cell formation.
  • Graafian follicle - named after Regnier de Graaf (1641-1673), an historic Dutch physician embryologist who studied pregnancy using rabbits.
  • granulosa cells - the supporting cells that surround the developing egg within the follicle thecal layers.
  • homologs - maternal and paternal homologous chromosomes.
  • Izumo1 - a protein located on the equatorial segment of acrosome-reacted spermatozoa recognizes its receptor Juno, on the oocyte surface, for plasma membrane binding and fusion. Named for a Japanese shrine dedicated to marriage. OMIM609278
  • Juno - (folate receptor-δ; FOLR-δ) a glycophosphatidylinositol (GPI)-anchored, cysteine-rich glycoprotein on the oocyte surface for fertilisation that is the receptor of Izumo1 on the spermatozoa, for plasma membrane binding and fusion. OMIM615737
  • luteinizing hormone - (LH, gonadotropin, lutropin, Interstitial Cell Stimulating Hormone, ICSH) glycoprotein hormone releasd from anterior pituitary hormone that acts on the gonad and has a role in male and female reproduction. Female, LH triggers ovulation (release of the oocyte). Male, LH stimulates testis interstital cell (Leydig cell) production of testosterone. Have been used clinically in humans for the treatment of female infertility.
  • meiosis - oocyte reductive (diploid to haploid) cell division, with 1 round of DNA replication is followed by 2 rounds of chromosome segregation. The process beginning in the fetus and only completed at fertilization.
  • mesovarium - mesentry of the ovary formed from a fold of the broad ligament that attaches the ovary.
  • medullary - (L. medius = in the middle) relating to the medulla; pith, marrow, inner portion of an organ. Usually combined with cortex (cortical) meaning the outer layer.
  • oocyte - (Greek, oo = egg, ovum) The term used to describe the haploid egg or ovum formed within the ovary (female gonad) and released to enter the uterine tube and be transported to the uterus. The mature oocyte is the cell released from the ovary during ovulation.
  • oogenesis - (Greek, oo = egg + genesis = origin, creation, generation) process of diploid oogonia division and differentiation into an haploid oocyte (egg) within the ovary (female gonad). Mammalian meiosis will only be completed within the oocyte if fertilization occurs.
  • oogonia - (Greek, oo = egg) diploid germ cells within the ovary (female gonad) which provide the primary oocytes for oocyte (egg) formation. In humans, all oogonia form primary oocytes within the ovary before birth.
  • oolemma - (zona pellucida, vitelline membrane).
  • oophorus - (Greek, oo = egg + phorus = carrying, egg-bearing) cumulus oophorus, used to describe the granulosa cells within the follicle that tether or link the oocyte to the wall of the follicle.
  • ovarian reserve - Clinical term for the number of oocytes (non-growing follicles) available for possible fertilization at the different times during female reproductive life. A blood test for Anti-Mullerian Hormone (AMH) levels is used clinically as a measure of the ovarian reserve. human graph
  • ovastacin - an oocyte released enzyme following fertilization that cleaves ZP2 protein to prevent polyspermy.
  • ovulation - release of the oocyte from the mature follicle. In humans generally a single oocyte is released from a cohort of several maturing follicles.
  • ovum - oocyte, note that historically this same term was also used to describe the early stages following fertilisation.
  • polyspermy - abnormal fertilization by more that a single spermatozoa, may generate a hydatidiform mole.
  • preantral follicle - (primary) the stage following primordial in the description of the sequence ovarian follicle development.
  • primary follicle - (preantral) the stage following primordial in the description of the sequence ovarian follicle development.
  • primordial follicle - the first stage in the description of the sequence ovarian follicle development. Present in the ovary from birth, located in the stroma of the ovary cortex beneath the tunica albuginea. The primordial follicle is the oocyte and the surrounding follicular cells.
  • primordial germ cell - oocyte present in the primordial follicle ovary from birth, located in the stroma of the ovary cortex beneath the tunica albuginea. The primordial follicle is the oocyte and the surrounding follicular cells.
  • secondary follicles - the stage following primary in the description of the sequence ovarian follicle development.
  • stromal cells - in the ovary, cells surrounding the developing follicle that form a connective tissue sheath (theca folliculi). This layer then differentiates into 2 layers (theca interna, theca externa). This region is richly vascularized and involved in hormone secretion.
  • superovulation therapy - a fertility drug treatement (oral clomiphene citrate and/or injectable FSH with or without LH) aimed at stimulating development/release of more than one follicle during a single menstrual cycle.
  • tertiary follicle - (preovulatory, Graffian) the stage following secondary in the description of the sequence ovarian follicle development.
  • theca folliculi - stromal cells in the ovary, cells surrounding the developing follicle that form a connective tissue sheath. This layer then differentiates into 2 layers (theca interna, theca externa). This region is vascularized and involved in hormone secretion.
  • theca externa - stromal cells forming the outer layer of the theca folliculi surrounding the developing follicle. Consisting of connective tissue cells, smooth muscle and collagen fibers.
  • theca interna - stromal cells forming the inner layer of the theca folliculi surrounding the developing follicle. This vascularized layer of cells respond to LH (leutenizing hormone) synthesizing and secreting androgens which are processed into estrogen.
  • transzonal projection - (TZP) ovarian follicle term describing the cellular membraneous extension from the granulosa cell through the zona pellucida to the oocyte cell membrane where it forms gap junctions or adherens junctions allowing signalling and adhesion between the two cells.
  • tunica albuginea - dense connective tissue layer lying between germinal epithelium and cortical region of ovary.
  • uterus - site of embryo implantation and development. Uterine wall has 3 major layers: endometrium, myometrium, and perimetrium. Endometrium can be further divided into the functional layer (shed/lost during menstruation) and basal layer (not lost during menstruation).
  • zinc sparks following fertilization the oocyte releases a burst of zinc atoms in brief bursts (zinc sparks) has a role in zonal pellucida induced structural changes (hardening) along with ovastacin cleavage of ZP2 protein.
  • zona hardening - following fertilization the structural changes that occur to the zona pellucida to prevents further spermatozoa binding acting as a block to polyspermy.
  • zona pellucida - extracellular layer lying directly around the oocyte underneath follicular cells. Has an important role in egg development, fertilization and blastocyst development. This thick extracellular matrix consists of glcosaminoglycans and 3 glycoproteins (ZP1, ZP2, ZP3). (More? Zona pellucida)
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Cell Division Terms  
Meiosis | Mitosis
  • anaphase - (Greek, ana = up, again) Mitosis term referring to the fourth stage, where the paired chromatids now separate and migrate to spindle poles. This is followed by telophase.
  • anaphase A - Mitosis term referring to the part of anaphase during which the chromosomes move.
  • anaphase B - Mitosis term referring to the part of anaphase during which the poles of the mitotic spindle move apart.
  • aneuploidy - (aneuploid) term used to describe an abnormal number of chromosomes mainly (90%) due to chromosome malsegregation mechanisms in maternal meiosis I.
  • aster - (Latin, aster = star) star-like object visible in most dividing eukaryotic cells contains the microtubule organizing center.
  • astral microtubule - spindle apparatus microtubule (MT) originating from the centrosome which does not connect to a kinetochore. These microtubules only exist during mitosis, the other spindle types are polar and kinetochore microtubules.
  • autosomal inheritance - term used in hereditary diseases which means that the disease is due to a DNA error in one of the 22 chromosome pairs that are not sex chromosomes. Both boys and girls can then inherit this error. If the error is in a sex chromosome, the inheritance is said to be sex-linked.
  • bivalent - (tetrad) a pair of homologous chromosomes physically held together by at least one DNA crossover.
  • bouquet stage - meiosis term for when in prophase transition to the zygotene stage, the chromosome telomeres attachment to the inner nuclear envelope and form a cluster. This occurs before the onset of homologous pairing and synapsis. The name comes from the chromosomes resembling a "bouquet of flowers".
  • diploid - (Greek, di = double + ploion = vessel) having two sets of chromosomes (2n), this is the normal euploidy state for all human cells, other than gametes that are haploid (n, a single set of chromosomes).
  • diplotene stage- (diplotene phase, diplonema; Greek, diplonema = "two threads") meiotic stage seen during prophase I, the chromosomes separate from one another a small amount giving this appearance. In the developing human ovary, oocytes remain at the diplotene stage from fetal life through postnatal childhood, until puberty when the lutenizing hormone (LH) surges stimulate the resumption of meiosis. Prophase I, is divided into 5 stages (leptotene, zygotene, pachytene, diplotene, diakinesis) based upon changes associated with the synaptonemal complex structure that forms between two pairs of homologous chromosomes.
  • euploidy - the normal genome chromosomal set (n, 2n, 3n) or complement for a species, in humans this is diploid (2n). The other classes of numerical chromosomal abnormalities include aneuploidy, polyploidy and mixoploidy.
  • FUCCI - Acronym for Fluorescence Ubiquitination Cell Cycle Indicator a molecular tool for identifying the stage in the cell cycle. In G0/G1 cells express a red fluorescent protein and S/G2/M cells express a green fluorescent protein. (More? Tooth Development Movie)
  • haploid - (Greek, haploos = single) Having a single set of chromosomes (n) as in mature germ/sex cells (oocyte, spermatozoa) following reductive cell division by meiosis. Normally cells are diploid, containing 2 sets of chromosomes. Ploidy refers to the number of sets of chromosomes in the nucleus of a cell.
  • heteroplasmy - presence of more than one type of organellar genome. In humans this can refer to variations in the mitochondrial DNA (mtDNA). (More? PMID 26281784)
  • homologous chromosomes - meiosis term for the two matching (maternal and one paternal) chromosomes that align during meiosis I.
  • homologous recombination - meiosis term when DNA of homologous chromosomes is covalently exchanged to produce chromosomes with new allele combinations, and also links homologous chromosomes with each other to form a bivalent
  • human genome - DNA within the 23 nucleus chromosome pairs and the cytoplasmic mitochondrial DNA.
  • kinetochore - the protein structure formed on chromatids where the spindle kinetochore microtubules attach during cell division.
  • kinetochore microtubule - spindle apparatus microtubule (MT) that attaches to the chromosome kinetochore by its plus end, the other spindle types are astral and polar microtubules.
  • kinesin - a microtubule (MT) motor protein that exists in many isoforms and most move towards the MT positive end. Different isoforms have different functions within the spindle apparatus. PMID 20109570
  • meiosis - reductive cell division required to produce germ cells (oocyte, spermatozoa) and for sexual reproduction. Note that only spermatozoa complete meiosis before fertilisation. Chromosome number is reduced from diploid to haploid, during this process maternal and paternal genetic material are exchanged. All other non-germ cells in the body divide by mitosis. (More? Meiosis | Spermatozoa Development | Oocyte Development | Week 1)
  • meiosis I - (MI) the first part of meiosis resulting in separation of homologous chromosomes, in humans producing two haploid cells (N chromosomes, 23), a reductional division.
  • meiosis II - (MII) the second part of meiosis. In male human spermatogenesis, producing of four haploid cells (23 chromosomes, 1N) from the two haploid cells (23 chromosomes, 1N), each of the chromosomes consisting of two sister chromatids produced in meiosis I. In female human oogenesis, only a single haploid cell (23 chromosomes, 1N) is produced. Meiosis II: Prophase II - Metaphase II - Anaphase II - Telophase II.
  • meiotic silencing of unsynapsed chromatin - (MSUC) an aneuploidy protective mechanism for subsequent generations, during meiosis where chromosomes are silenced that fail to pair with their homologous partners.
  • merotelic kinetochore - cell division abnormality in chromosomal attachment that occurs when a single kinetochore is attached to microtubules arising from both spindle poles. Normal chromosomal attachment in early mitosis, is by only one of the two sister kinetochores attached to spindle microtubules (monotelic attachment) later sister kinetochores attach to microtubules arising from opposite spindle poles (amphitelic attachment).
  • metaphase - mitosis term referring to the third stage where mitotic spindle kinetochore microtubules align chromosomes in one midpoint plane. Metaphase ends when sister kinetochores separate. Originally based on light microscopy of living cells and electron microscopy of fixed and stained cells. A light microscope analysis called a "metaphase spread" was originally used to detect chromosomal abnormalities in cells. Mitosis Phases: prophase - prometaphase - metaphase - anaphase - telophase
  • metaphase spread - In mitosis using light microscope analysis originally used to detect chromosomal abnormalities in cells, as chromosomes are only visible during cell division.
  • microfilament - (MF) cytoskeleton filament normally required for cytoplasmic intracellular transport, motility and cell shape. Named by the actin monomers assembling into the smallest in cross-section of the three filament systems (microtubules and intermediate filaments). This system is disassembled and reassembled as the contractile ring for cytokinesis (cytoplasm division) following cell division mitosis and meiosis.
  • microtubule - (MT) cytoskeleton filament normally required for cytoplasmic intracellular transport and motility. Named by the tubulin monomers assembling into "tubes", and are the largest in cross-section of the three filament systems (microfilaments and intermediate filaments). This system is disassembled and reassembled as the spindle apparatus during cell division.
  • mitochondrial DNA - (mtDNA) multiple copies of a small circular DNA molecule located within the mitochondria matrix. In humans 16,568 bp in length containing 37 genes, originally inherited only from the oocyte (maternal inheritance).
  • mitosis - (M phase) The normal division of all cells, except germ cells, where chromosome number is maintained (diploid). In germ cell division (oocyte, spermatozoa) meiosis is a modified form of this division resulting in reduction in genetic content (haploid). Mitosis, division of the nucleus, is followed by cytokinesis the division of the cell cytoplasm and the cytoplasmic contents. cytokinesis overlaps with telophase.
  • p - chromosome short arm (possibly French, petit) and used along with chromosome and band number to indicate genes located on this arm of the chromosome. The chromosome long arm is identified as q (possibly French, tall) chosen as next letter in alphabet after p. These chromosomal arms are only seen when the chromosome is folded for cell division.
  • polar microtubule - spindle apparatus microtubule (MT) that can arise from either pole and overlap at the spindle midzone. This interdigitating structure consisting of antiparallel microtubules is responsible for pushing the poles of the spindle apart. The other spindle types are astral and kinetochore microtubules.
  • prometaphase - (Greek, pro = before) mitosis term referring to the second stage, when the nuclear envelope breaks down into vesicles. Microtubules then extend from the centrosomes at the spindle poles (ends) and reach the chromosomes. This is followed by metaphase.
  • pronuclear fusion - (Greek, pro = before) the process of the fusion of the two haploid nuclear structures (pronuclei) contributed from the spermatazoa and oocyte to form the first diploid nucleus cell. Can also be called "fusion of pronuclei".
  • pronucleus - (Greek, pro = before; plural, pronuclei) the two haploid nuclei or nuclear structures containing the genetic material from the spermatozoa and the oocyte. These two haploid nuclei will fuse together to form the first diploid nucleus cell, the zygote. Therefore the nuclear structures that exist "before the nucleus", the plural term is pronuclei.
  • prophase - (Greek, pro = before) - mitosis term referring to the first stage, when the diffusely stained chromatin resolves into discrete chromosomes, each consisting of two chromatids joined together at the centromere.
  • prophase I - meiosis term refers to the first phase of meiosis I, which together with meiosis II results in the reductive cell division only occurring gametes. Prophase can be further divided into a number of stages: leptotene zygotene, pachytene, diplotene, diakinesis.
  • q - chromosome long arm (possibly French, tall), the next letter in alphabet after p, and used along with chromosome and band number to indicate genes located on this arm of the chromosome. The chromosome short arm is identified as p (possibly French, petit). These chromosomal arms are only seen when the chromosome is folded for cell division.
  • S phase - during interphase of cell cycle where DNA is duplicated prior to second growth period (G2 phase) that is followed by mitosis (M phase).
  • synapsis - (syndesis) meiosis term for the pairing of two homologous chromosomes that occurs during prophase I.
  • synaptonemal complex - meiosis term for a protein structure essential for synapsis of homologous chromosomes. (proteins SCP3 and SCP1).
  • telomere - region found at each end of the chromosome and involved in cellular ageing and the capacity for division. The regions consist of repeated sequences protecting the ends of chromosomes and harbour DNA repair proteins. In the absence of the enzyme telomerase, these regions shorten during each cell division and becoming critically short, cell senescence occurs.
  • telophase - mitosis term referring to the fifth stage, where the vesicles of the nuclear envelope reform around the daughter cells, the nucleoli reappear and the chromosomes unfold to allow gene expression to begin. This phase overlaps with cytokinesis, the division of the cell cytoplasm.
  • telomerase - the enzyme that maintains the chromosome end length, the telomeres, involved in cellular ageing and the capacity for division. Absence of telomerase activity leads to the chromosome ends shorten during each cell division, becoming critically short and cell senescence then occurs.
  • tetrad - (bivalent) a pair of homologous chromosomes physically held together by at least one DNA crossover.
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Cite this page: Hill, M.A. (2018, September 23) Embryology Oocyte Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Oocyte_Development

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