Reactive oxygen species as mediators of sperm capacitation and pathological damage

Robert J. Aitken

doi:10.1002/mrd.22871

journal article Sep 05, 2017

Reactive oxygen species as mediators of sperm capacitation and pathological damage

Robert J. Aitken

Molecular Reproduction and Development Vol. 84 No. 10 pp. 1039-1052 · Wiley

View at Publisher Save 10.1002/mrd.22871

Abstract

Oxidative stress plays a major role in the life and death of mammalian spermatozoa. These gametes are professional generators of reactive oxygen species (ROS), which appear to derive from three potential sources: sperm mitochondria, cytosolic L‐amino acid oxidases, and plasma membrane Nicotinamide adenine dinucleotide phosphate oxidases. The oxidative stress created via these sources appears to play a significant role in driving the physiological changes associated with sperm capacitation through the stimulation of a cyclic adenosine monophosphate/Protein kinase A phosphorylation cascade, including the activation of Extracellular signal regulated kinase‐like proteins, massive up‐regulation of tyrosine phosphorylation in the sperm tail, as well as the induction of sterol oxidation. When generated in excess, however, ROS can induce lipid peroxidation that, in turn, disrupts membrane characteristics that are critical for the maintenance of sperm function, including the capacity to fertilize an egg. Furthermore, the lipid aldehydes generated as a consequence of lipid peroxidation bind to proteins in the mitochondrial electron transport chain, triggering yet more ROS generation in a self‐perpetuating cycle. The high levels of oxidative stress created as a result of this process ultimately damage the DNA in the sperm nucleus; indeed, DNA damage in the male germ line appears to be predominantly induced oxidatively, reflecting the vulnerability of these cells to such stress. Extensive evaluation of antioxidants that protect the spermatozoa against oxidative stress while permitting the normal reduction‐oxidation regulation of sperm capacitation is therefore currently being undertaken, and has already proven efficacious in animal models.

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References

129

[1]

10.1095/biolreprod.111.092528

[2]

10.4103/1008-682x.153850

[3]

10.1002/j.1939-4640.2004.tb02815.x

[4]

10.1002/jcp.1041510305

[5]

10.1530/jrf.0.0810459

[6]

10.1095/biolreprod41.1.183

[7]

10.1089/ars.2010.3186

[8]

10.1093/molehr/gap059

[9]

10.1093/humrep/deu204

[10]

10.1002/(sici)1098-2795(199708)47:4<468::aid-mrd14>3.0.co;2-s

[11]

10.1111/andr.12157

[12]

10.1002/mrd.1080350313

[13]

Aitken R. J. "A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox‐regulated, cAMP‐mediated induction of tyrosine phosphorylation" Journal of Cell Science (1998) 10.1242/jcs.111.5.645

[14]

Aitken J. B. "Characterization of an L‐amino acid oxidase in equine spermatozoa" Biology of Reproduction (2015)

[15]

10.1093/molehr/gat067

[16]

Aitken R. J. "Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function" Journal of Cell Science (1995) 10.1242/jcs.108.5.2017

[17]

10.1016/j.freeradbiomed.2004.01.017

[18]

10.1210/jc.2006-1309

[19]

10.1074/jbc.m112.366690

[20]

10.1002/j.1939-4640.1987.tb00973.x

[21]

10.1016/j.anireprosci.2013.03.016

[22]

10.1071/bi9510581

[23]

10.1242/jcs.03055

[24]

10.1016/j.ydbio.2009.06.022

[25]

10.1093/molehr/gat033

[26]

10.1016/s0093-691x(01)00710-5

[27]

10.1002/mrd.20285

[28]

Bielski B. H. J. "A study of the reactivity of HO2/O2 ‐. with unsaturated fatty acids" The Journal of Biological Chemistry (1983) 10.1016/s0021-9258(18)32488-8

[29]

10.1095/biolreprod44.3.398

[30]

10.1095/biolreprod.112.101253

[31]

10.1093/biolre/iox005

[32]

10.1074/jbc.m116.738930

[33]

10.1111/and.12301

[34]

10.1111/j.1365-2605.2009.00971.x

[35]

10.1038/168697b0

[36]

10.1161/circresaha.114.300559

[37]

10.1016/j.theriogenology.2005.06.015

[38]

10.1002/j.1939-4640.1997.tb01953.x

[39]

10.1073/pnas.78.12.7560

[40]

10.1111/j.1365-2605.1993.tb01148.x

[41]

10.1016/0891-5849(94)00169-k

[42]

de Lamirande E. "Human sperm capacitation induced by biological fluids and progesterone, but not by NADH or NADPH, is associated with the production of superoxide anion" Journal of Andrology (1998) 10.1002/j.1939-4640.1998.tb01991.x

[43]

10.1530/ror.0.0020048

[44]

10.1095/biolreprod.109.076836

[45]

10.1210/jc.2005-2711

[46]

10.1016/j.ejphar.2013.12.033

[47]

10.1093/humrep/der321

[48]

10.1095/biolreprod.102.012716

[49]

10.1530/rep.1.00646

[50]

10.1530/jrf.0.0610025

Showing 50 of 129 references

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Metrics

522

Citations

129

References

Details

Published: Sep 05, 2017
Vol/Issue: 84(10)
Pages: 1039-1052
License: View

Authors

R

Robert J. Aitken

Discipline of Biological Sciences Priority Research Centre in Reproductive Science The University of Newcastle Callaghan NSW Australia

Funding

National Health and Medical Research Council Award: NHMRC Discovery Grant 401267

University of Newcastle Australia Award: Priority Research Centre for Reproductive Science

Cite This Article

Robert J. Aitken (2017). Reactive oxygen species as mediators of sperm capacitation and pathological damage. Molecular Reproduction and Development, 84(10), 1039-1052. https://doi.org/10.1002/mrd.22871

Reactive oxygen species as mediators of sperm capacitation and pathological damage

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