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Meiotic Instability Generates a Pathological Condition in Mammalian Ovum

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Abstract

Maintenance of metaphase-II (M-II) arrest in ovum is required to present itself as a right gamete for successful fertilization in mammals. Surprisingly, instability of meiotic cell cycle results in spontaneous exit from M-II arrest, chromosomal scattering and incomplete extrusion of second polar body (PB-II) without forming pronuclei so called abortive spontaneous ovum activation (SOA). It remains unclear what causes meiotic instability in freshly ovulated ovum that results in abortive SOA. We propose the involvement of various signal molecules such as reactive oxygen species (ROS), cyclic 3′,5′ adenosine monophosphate (cAMP) and calcium (Ca2+) in the induction of meiotic instability and thereby abortive SOA. These signal molecules through their downstream pathways modulate phosphorylation status and activity of cyclin dependent kinase (cdk1) as well as cyclin B1 level. Changes in phosphorylation status of cdk1 and its activity, dissociation and degradation of cyclin B1 destabilize maturation promoting factor (MPF). The premature MPF destabilization and defects in other cell cycle regulators possibly cause meiotic instability in ovum soon after ovulation. The meiotic instability results in a pathological condition of abortive SOA and deteriorates ovum quality. These ova are unfit for fertilization and limit reproductive outcome in several mammalian species including human. Therefore, global attention is required to identify the underlying causes in greater details in order to address the problem of meiotic instability in ova of several mammalian species icluding human. Moreover, these activated ova may be used to create parthenogenetic embryonic stem cell lines in vitro for the use in regenerative medicine.

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Abbreviations

M-II:

metaphase-II

M-III:

metaphase-III

SOA:

spontaneous ovum activation

ROS:

Reactive oxygen species

cAMP:

cyclic 3′,5′ adenosine monophosphate

Ca2+ :

calcium

cdk1:

cyclin- dependent kinase

MPF:

maturation promoting factor

PB-I:

first polar body

PB-II:

second polar body

Emi2:

early meittic inhibitor 2

MAPK:

mitogen activated protein kinase

MMP:

Mitochondrial membrane potential

ΔΨm:

negative trans-membrane potential of mitochondria

H2O2 :

hydrogen peroxide

CaMK-II:

CaM-dependent kinase-II

CSFs:

cytostatic factors including

APC/C:

anaphase promoting complex/cyclosome

MAD2:

mitotic arrest deficient protein

ARTs:

assisted reproductive technologies

IVF:

in vitro fertilization

ICSI:

intra-cytoplasmic sperm injection

SCNT:

somatic cell nuclear transfer

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Funding

This study was financially supported by Department of Biotechnology, Ministry of Science and Technology, Government of India (Grant no. BT/PR4225/AAQ/1/492/2011).

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Authors and Affiliations

  1. Cell Physiology Laboratory, Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Karuppanan V. Premkumar, Meenakshi Tiwari, Ashutosh N. Pandey, Anumegha Gupta, Alka Sharma, Pramod K. Yadav, Anil K. Yadav, Devendra K. Pandey & Shail K. Chaube

  2. Amity Institute of Biotechnology, Amity University Jharkhand, Ranchi, 834001, India

    Shilpa Prasad

  3. Department of Kayachikitsa, Faculty of Ayurveda, Institute of Medical Sciences, Banaras Hindu University, Varanasi, 221005, India

    Ajai K. Pandey

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KVP, SP suggested the structure. DKP searched the literature and MT, ANP wrote the initial draft of manuscript. AG, AS, PKY, AKY and AKP revised and finished the final version of manuscript under the supervision of SKC. All authors read and approved the final manuscript.

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Correspondence to Shail K. Chaube.

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Premkumar, K.V., Prasad, S., Tiwari, M. et al. Meiotic Instability Generates a Pathological Condition in Mammalian Ovum. Stem Cell Rev and Rep 17, 777–784 (2021). https://doi.org/10.1007/s12015-020-10072-z

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