Cytoplasmic maturation of bovine oocytes: Structural and biochemical modifications and acquisition of developmental competence

Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner, ultimately reaching activation of the embryonic genome. This process involves complex and distinct, although linked, events of nuclear and cy...

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Published inTheriogenology Vol. 71; no. 5; pp. 836 - 848
Main Authors Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A., Navarro, P.A.A.S.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.03.2009
[Oxford]: Butterworth-Heinemann; [New York]: Elsevier Science
Subjects
Online AccessGet full text
ISSN0093-691X
1879-3231
DOI10.1016/j.theriogenology.2008.10.023

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Abstract Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner, ultimately reaching activation of the embryonic genome. This process involves complex and distinct, although linked, events of nuclear and cytoplasmic maturation. Nuclear maturation mainly involves chromosomal segregation, whereas cytoplasmic maturation involves organelle reorganization and storage of mRNAs, proteins and transcription factors that act in the overall maturation process, fertilization and early embryogenesis. Thus, for didactic purposes, we subdivided cytoplasmic maturation into: (1) organelle redistribution, (2) cytoskeleton dynamics, and (3) molecular maturation. Ultrastructural analysis has shown that mitochondria, ribosomes, endoplasmic reticulum, cortical granules and the Golgi complex assume different positions during the transition from the germinal vesicle stage to metaphase II. The cytoskeletal microfilaments and microtubules present in the cytoplasm promote these movements and act on chromosome segregation. Molecular maturation consists of transcription, storage and processing of maternal mRNA, which is stored in a stable, inactive form until translational recruitment. Polyadenylation is the main mechanism that initiates protein translation and consists of the addition of adenosine residues to the 3′ terminal portion of mRNA. Cell cycle regulators, proteins, cytoplasmic maturation markers and components of the enzymatic antioxidant system are mainly transcribed during this stage. Thus, the objective of this review is to focus on the cytoplasmic maturation process by analyzing the modifications in this compartment during the acquisition of meiotic competence for development.
AbstractList Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner, ultimately reaching activation of the embryonic genome. This process involves complex and distinct, although linked, events of nuclear and cytoplasmic maturation. Nuclear maturation mainly involves chromosomal segregation, whereas cytoplasmic maturation involves organelle reorganization and storage of mRNAs, proteins and transcription factors that act in the overall maturation process, fertilization and early embryogenesis. Thus, for didactic purposes, we subdivided cytoplasmic maturation into: (1) organelle redistribution, (2) cytoskeleton dynamics, and (3) molecular maturation. Ultrastructural analysis has shown that mitochondria, ribosomes, endoplasmic reticulum, cortical granules and the Golgi complex assume different positions during the transition from the germinal vesicle stage to metaphase II. The cytoskeletal microfilaments and microtubules present in the cytoplasm promote these movements and act on chromosome segregation. Molecular maturation consists of transcription, storage and processing of maternal mRNA, which is stored in a stable, inactive form until translational recruitment. Polyadenylation is the main mechanism that initiates protein translation and consists of the addition of adenosine residues to the 3' terminal portion of mRNA. Cell cycle regulators, proteins, cytoplasmic maturation markers and components of the enzymatic antioxidant system are mainly transcribed during this stage. Thus, the objective of this review is to focus on the cytoplasmic maturation process by analyzing the modifications in this compartment during the acquisition of meiotic competence for development.
Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner, ultimately reaching activation of the embryonic genome. This process involves complex and distinct, although linked, events of nuclear and cytoplasmic maturation. Nuclear maturation mainly involves chromosomal segregation, whereas cytoplasmic maturation involves organelle reorganization and storage of mRNAs, proteins and transcription factors that act in the overall maturation process, fertilization and early embryogenesis. Thus, for didactic purposes, we subdivided cytoplasmic maturation into: (1) organelle redistribution, (2) cytoskeleton dynamics, and (3) molecular maturation. Ultrastructural analysis has shown that mitochondria, ribosomes, endoplasmic reticulum, cortical granules and the Golgi complex assume different positions during the transition from the germinal vesicle stage to metaphase II. The cytoskeletal microfilaments and microtubules present in the cytoplasm promote these movements and act on chromosome segregation. Molecular maturation consists of transcription, storage and processing of maternal mRNA, which is stored in a stable, inactive form until translational recruitment. Polyadenylation is the main mechanism that initiates protein translation and consists of the addition of adenosine residues to the 3' terminal portion of mRNA. Cell cycle regulators, proteins, cytoplasmic maturation markers and components of the enzymatic antioxidant system are mainly transcribed during this stage. Thus, the objective of this review is to focus on the cytoplasmic maturation process by analyzing the modifications in this compartment during the acquisition of meiotic competence for development.Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner, ultimately reaching activation of the embryonic genome. This process involves complex and distinct, although linked, events of nuclear and cytoplasmic maturation. Nuclear maturation mainly involves chromosomal segregation, whereas cytoplasmic maturation involves organelle reorganization and storage of mRNAs, proteins and transcription factors that act in the overall maturation process, fertilization and early embryogenesis. Thus, for didactic purposes, we subdivided cytoplasmic maturation into: (1) organelle redistribution, (2) cytoskeleton dynamics, and (3) molecular maturation. Ultrastructural analysis has shown that mitochondria, ribosomes, endoplasmic reticulum, cortical granules and the Golgi complex assume different positions during the transition from the germinal vesicle stage to metaphase II. The cytoskeletal microfilaments and microtubules present in the cytoplasm promote these movements and act on chromosome segregation. Molecular maturation consists of transcription, storage and processing of maternal mRNA, which is stored in a stable, inactive form until translational recruitment. Polyadenylation is the main mechanism that initiates protein translation and consists of the addition of adenosine residues to the 3' terminal portion of mRNA. Cell cycle regulators, proteins, cytoplasmic maturation markers and components of the enzymatic antioxidant system are mainly transcribed during this stage. Thus, the objective of this review is to focus on the cytoplasmic maturation process by analyzing the modifications in this compartment during the acquisition of meiotic competence for development.
Author Ferriani, R.A.
Navarro, P.A.A.S.
Vireque, A.A.
Adona, P.R.
Ferreira, E.M.
Meirelles, F.V.
Author_xml – sequence: 1
  givenname: E.M.
  surname: Ferreira
  fullname: Ferreira, E.M.
  email: elisamferreira@yahoo.com.br
  organization: Department of Gynecology and Obstetrics, Faculty of Medicine of Ribeirão Preto, University of São Paulo, 14048-900 Ribeirão Preto, SP, Brazil
– sequence: 2
  givenname: A.A.
  surname: Vireque
  fullname: Vireque, A.A.
  organization: Department of Gynecology and Obstetrics, Faculty of Medicine of Ribeirão Preto, University of São Paulo, 14048-900 Ribeirão Preto, SP, Brazil
– sequence: 3
  givenname: P.R.
  surname: Adona
  fullname: Adona, P.R.
  organization: Department of Basic Sciences, Faculty of Zootechny and Aliments Engeneering, University of São Paulo, 13630-970 Pirassununga, SP, Brazil
– sequence: 4
  givenname: F.V.
  surname: Meirelles
  fullname: Meirelles, F.V.
  organization: Department of Basic Sciences, Faculty of Zootechny and Aliments Engeneering, University of São Paulo, 13630-970 Pirassununga, SP, Brazil
– sequence: 5
  givenname: R.A.
  surname: Ferriani
  fullname: Ferriani, R.A.
  organization: Department of Gynecology and Obstetrics, Faculty of Medicine of Ribeirão Preto, University of São Paulo, 14048-900 Ribeirão Preto, SP, Brazil
– sequence: 6
  givenname: P.A.A.S.
  surname: Navarro
  fullname: Navarro, P.A.A.S.
  organization: Department of Gynecology and Obstetrics, Faculty of Medicine of Ribeirão Preto, University of São Paulo, 14048-900 Ribeirão Preto, SP, Brazil
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19121865$$D View this record in MEDLINE/PubMed
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Snippet Oocyte maturation is a long process during which oocytes acquire their intrinsic ability to support the subsequent stages of development in a stepwise manner,...
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SubjectTerms animal proteins
Animals
Bovine oocytes
Cattle
chromosome segregation
cytochemistry
cytoplasm
Cytoplasm - chemistry
Cytoplasm - physiology
Cytoplasmic maturation
Cytoskeleton
Cytoskeleton - physiology
Cytoskeleton - ultrastructure
developmental competence
developmental stages
Female
Golgi apparatus
literature reviews
Meiosis
messenger RNA
microtubules
mitochondria
Molecular maturation
oocyte maturation
oocytes
Oocytes - growth & development
Oocytes - metabolism
Oocytes - ultrastructure
Organelles
Organelles - physiology
Organelles - ultrastructure
ribosomes
RNA, Messenger - genetics
RNA, Messenger - metabolism
sarcoplasmic reticulum
transcription factors
ultrastructure
Title Cytoplasmic maturation of bovine oocytes: Structural and biochemical modifications and acquisition of developmental competence
URI https://dx.doi.org/10.1016/j.theriogenology.2008.10.023
https://www.ncbi.nlm.nih.gov/pubmed/19121865
https://www.proquest.com/docview/46199465
https://www.proquest.com/docview/66933094
Volume 71
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