Skip to main content

Advertisement

SpringerLink
Log in

Ageing associated proteomic variations in seminal plasma of Indian men

  • Original Article
  • Published:
Journal of Proteins and Proteomics Aims and scope Submit manuscript

Abstract

Background

Recent decade has seen a significant increase in the average age at which couples first produce, thus it becomes essential to study and understand how age affects fertility in humans.

Methodology

Age-dependent variations in human seminal plasma proteome were identified by two- dimensional differential gel electrophoresis (2D-DiGE) followed by mass spectrometric analysis.

Results

Overall, 10 differentially expressed proteins were identified, viz. glutaredoxin domain-containing cysteine-rich protein-2, clusterin, serum albumin, translation initiation factor IF-2 like, alternative protein RRT-34, ecto-ADP-ribosyltransferase 4, protein Unc-119 homolog A, CB1 cannabinoid receptor-interacting protein 1 and serotransferrin. Expression of clusterin was found upregulated in older age samples, which was further validated by western blotting analysis. It is evident from available literature that higher expression of clusterin is associated with poor semen quality.

Conclusion

Based on this, our study for some extent concludes and supports the fact that semen quality declines with increasing age.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CBB:

Coomassie brilliant blue

DiGE:

Differential gel electrophoresis

ROS:

Reactive oxygen species

References

  • Agarwal A, Makker K, Sharma R (2008) Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 59:2–11

    Article  CAS  PubMed  Google Scholar 

  • Agarwal A, Ayaz A, Samanta L, Sharma R, Assidi M, Abuzenadah AM, Sabanegh E (2015) Comparative proteomic network signatures in seminal plasma of infertile men as a function of reactive oxygen species. Clin Proteomics 12:23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahuja HS, Tenniswood M, Zakeri ZF (1996) Differential expression of clusterin in the testis and epididymis of postnatal and germ cell deficient mice. J Androl 17:491–501

    CAS  PubMed  Google Scholar 

  • Aitken RJ (2014) Age, the environment and our reproductive future: bonking baby boomers and the future of sex. Reproduction 147:S1–S11

    Article  CAS  PubMed  Google Scholar 

  • Aitken RJ, De Iuliis GN (2010) On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod 16:3–13

    Article  CAS  PubMed  Google Scholar 

  • Alam M, Selladurai M, Nagpal S, Tomar AK, Saraswat M, Raziuddin M, Mittal S, Singh TP, Yadav S (2010) Sample complexity reduction aids efficient detection of low-abundant proteins from human amniotic fluid. J Sep Sci 33:1723–1729

    Article  CAS  PubMed  Google Scholar 

  • Bailey R, Griswold MD (1999) Clusterin in the male reproductive system: localization and possible function. Mol Cell Endocrinol 151:17–23

    Article  CAS  PubMed  Google Scholar 

  • Belloc S, Cohen-Bacrie P, Benkhalifa M, Cohen-Bacrie M, De Mouzon J, Hazout A, Menezo Y (2008) Effect of maternal and paternal age on pregnancy and miscarriage rates after intrauterine insemination. Reprod Biomed Online 17:392–397

    Article  PubMed  Google Scholar 

  • Bieniek JM, Drabovich AP, Lo KC (2016) Seminal biomarkers for the evaluation of male infertility. Asian J Androl 18:426–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cadavid JA, Alvarez A, Markert UR, Cardona Maya W (2014) Differential protein expression in seminal plasma from fertile and infertile males. J Hum Reprod Sci 7(3):206–211

    Article  CAS  Google Scholar 

  • Cocuzza M, Athayde KS, Agarwal A, Sharma R, Pagani R, Lucon AM, Srougi M, Hallak J (2008) Age-related increase of reactive oxygen species in neat semen in healthy fertile men. Urology 71:490–494

    Article  PubMed  Google Scholar 

  • Cooper TG, Noonan E, von Eckardstein S, Auger J, Baker HW, Behre HM, Haugen TB, Kruger T, Wang C, Mbizvo MT, Vogelsong KM (2010) World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 16:231–245

    Article  PubMed  Google Scholar 

  • Cross NL (1998) Role of cholesterol in sperm capacitation. Biol Reprod 59:7–11

    Article  CAS  PubMed  Google Scholar 

  • Davalieva K, Kiprijanovska S, Noveski P, Plaseski T, Kocevska B, Broussard C, Plaseska-Karanfilska D (2012) Proteomic analysis of seminal plasma in men with different spermatogenic impairment. Andrologia 44:256–264

    Article  CAS  PubMed  Google Scholar 

  • Del Giudice PT, Belardin LB, Camargo M, Zylbersztejn DS, Carvalho VM, Cardozo KH, Bertolla RP, Cedenho AP (2016) Determination of testicular function in adolescents with varicocoele—a proteomics approach. Andrology 4:447–455

    Article  CAS  PubMed  Google Scholar 

  • Drabovich AP, Jarvi K, Diamandis EP (2011) Verification of male infertility biomarkers in seminal plasma by multiplex selected reaction monitoring assay. Mol Cell Proteom 10(M110):004127

    Google Scholar 

  • Drabovich AP, Saraon P, Jarvi K, Diamandis EP (2014) Seminal plasma as a diagnostic fluid for male reproductive system disorders. Nat Rev Urol 11:278–288

    Article  CAS  PubMed  Google Scholar 

  • Elzanaty S, Erenpreiss J, Becker C (2007) Seminal plasma albumin: origin and relation to the male reproductive parameters. Andrologia 39:60–65

    Article  CAS  PubMed  Google Scholar 

  • Ganguly S, Unisa S (2010) Trends of infertility and childlessness in India: findings from NFHS data. Facts Views Vis Obgyn 2(2):131–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N (2015) Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil 16:61–71

    PubMed  PubMed Central  Google Scholar 

  • Gray S, Huggins C (1942) Electrophoretic analysis of human semen. Proc Soc Exp Biol Med 50:351–353

    Article  CAS  Google Scholar 

  • Griffiths GS, Galileo DS, Aravindan RG, Martin-DeLeon PA (2009) Clusterin facilitates exchange of glycosyl phosphatidylinositol-linked SPAM1 between reproductive luminal fluids and mouse and human sperm membranes. Biol Reprod 81:562–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herwig R, Knoll C, Planyavsky M, Pourbiabany A, Greilberger J, Bennett KL (2013) Proteomic analysis of seminal plasma from infertile patients with oligoasthenoteratozoospermia due to oxidative stress and comparison with fertile volunteers. Fertil Steril 100(355–366):e352

    Google Scholar 

  • Humm KC, Sakkas D (2013) Role of increased male age in IVF and egg donation: is sperm DNA fragmentation responsible? Fertil Steril 99:30–36

    Article  CAS  PubMed  Google Scholar 

  • Intasqui P, Camargo M, Antoniassi MP, Cedenho AP, Carvalho VM, Cardozo KHM, Zylbersztejn DS, Bertolla RP (2016) Association between the seminal plasma proteome and sperm functional traits. Fertil Steril 105:617–628

    Article  CAS  PubMed  Google Scholar 

  • Johnson SL, Gemmell NJ (2012) Are old males still good males and can females tell the difference? Do hidden advantages of mating with old males off-set costs related to fertility, or are we missing something else? BioEssays 34:609–619

    Article  PubMed  Google Scholar 

  • Johnson SL, Dunleavy J, Gemmell NJ, Nakagawa S (2015) Consistent age-dependent declines in human semen quality: a systematic review and meta-analysis. Ageing Res Rev 19:22–33

    Article  PubMed  Google Scholar 

  • Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, Gudjonsson SA, Sigurdsson A, Jonasdottir A, Jonasdottir A, Wong WS, Sigurdsson G, Walters GB, Steinberg S, Helgason H, Thorleifsson G, Gudbjartsson DF, Helgason A, Magnusson OT, Thorsteinsdottir U, Stefansson K (2012) Rate of de novo mutations and the importance of father’s age to disease risk. Nature 488:471–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ (2008) Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab 93:3199–3207

    Article  CAS  PubMed  Google Scholar 

  • Kuhnert B, Nieschlag E (2004) Reproductive functions of the ageing male. Hum Reprod Update 10:327–339

    Article  PubMed  Google Scholar 

  • Li Y, Lin H, Li Y, Cao J (2011) Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil Steril 95:116–123

    Article  PubMed  Google Scholar 

  • Maheshwari A, Hamilton M, Bhattacharya S (2008) Effect of female age on the diagnostic categories of infertility. Hum Reprod 23:538–542

    Article  PubMed  Google Scholar 

  • Milardi D, Grande G, Vincenzoni F, Messana I, Pontecorvi A, De Marinis L, Castagnola M, Marana R (2012) Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil Steril 97:67–73

    Article  CAS  PubMed  Google Scholar 

  • Milardi D, Grande G, Vincenzoni F, Castagnola M, Marana R (2013) Proteomics of human seminal plasma: identification of biomarker candidates for fertility and infertility and the evolution of technology. Mol Reprod Dev 80:350–357

    Article  CAS  PubMed  Google Scholar 

  • Mostafa T, Anis T, El Nashar A, Imam H, Osman I (2012) Seminal plasma reactive oxygen species-antioxidants relationship with varicocele grade. Andrologia 44:66–69

    Article  CAS  PubMed  Google Scholar 

  • Pilch B, Mann M (2006) Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 7(5):R40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhardt K (2007) Evolutionary consequences of sperm cell aging. Q Rev Biol 82:375–393

    Article  PubMed  Google Scholar 

  • Salehi M, Akbari H, Heidari MH, Molouki A, Murulitharan K, Moeini H, Novin MG, Aabed F, Taheri H, Fadaei F, Mohsenzadeh M, Jafari M, Pirouzi A, Heidari R (2013) Correlation between human clusterin in seminal plasma with sperm protamine deficiency and DNA fragmentation. Mol Reprod Dev 80(9):718–724

    CAS  PubMed  Google Scholar 

  • Saraswat M, Joenvaara S, Jain T, Tomar AK, Sinha A, Singh S, Yadav S, Renkonen R (2017) Human spermatozoa quantitative proteomic signature classifies normo- and asthenozoospermia. Mol Cell Proteom 16:57–72

    Article  CAS  Google Scholar 

  • Sartorius GA, Nieschlag E (2010) Paternal age and reproduction. Hum Reprod Update 16:65–79

    Article  PubMed  Google Scholar 

  • Siva-Jothy MT (2000) The young sperm gambit. Ecol Lett 3:172–174

    Article  Google Scholar 

  • Song GJ, Lewis V (2008) Mitochondrial DNA integrity and copy number in sperm from infertile men. Fertil Steril 90:2238–2244

    Article  CAS  PubMed  Google Scholar 

  • Strocchi P, Smith MA, Perry G, Tamagno E, Danni O, Pession A, Gaiba A, Dozza B (2006) Clusterin up-regulation following sub-lethal oxidative stress and lipid peroxidation in human neuroblastoma cells. Neurobiol Aging 27:1588–1594

    Article  CAS  PubMed  Google Scholar 

  • Sylvester SR, Morales C, Oko R, Griswold MD (1991) Localization of sulfated glycoprotein-2 (clusterin) on spermatozoa and in the reproductive tract of the male rat. Biol Reprod 45:195–207

    Article  CAS  PubMed  Google Scholar 

  • Tomar AK, Sooch BS, Raj I, Singh S, Singh TP, Yadav S (2011) Isolation and identification of Concanavalin A binding glycoproteins from human seminal plasma: a step towards identification of male infertility marker proteins. Dis Mark 31:379–386

    Article  CAS  Google Scholar 

  • Tomar AK, Sooch BS, Singh S, Yadav S (2012) Differential proteomics of human seminal plasma: a potential target for searching male infertility marker proteins. Proteom Clin Appl 6:147–151

    Article  CAS  Google Scholar 

  • Tomar AK, Kumar S, Chhillar S, Kumaresan A, Singh S, Yadav S (2016) Human serum albumin and prolactin inducible protein complex enhances sperm capacitation in vitro. J. Proteins Proteom 7:107–113

    CAS  Google Scholar 

  • Wang J, Wang J, Zhang HR, Shi HJ, Ma D, Zhao HX, Lin B, Li RS (2009) Proteomic analysis of seminal plasma from asthenozoospermia patients reveals proteins that affect oxidative stress responses and semen quality. Asian J Androl 11:484–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jodar M, Soler-Ventura A, Oliva R, Molecular Biology of R. and Development Research G. (2017) Semen proteomics and male infertility. J Proteom 162:125–134

    Article  CAS  Google Scholar 

  • Yamakawa K, Yoshida K, Nishikawa H, Kato T, Iwamoto T (2007) Comparative analysis of interindividual variations in the seminal plasma proteome of fertile men with identification of potential markers for azoospermia in infertile patients. J Androl 28:858–865

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by research grant received from Indian Council for Medical Research (ICMR), Government of India, New Delhi. KK also acknowledges ICMR for his fellowship.

Author information

Authors and Affiliations

  1. Department of Biophysics, All India Institute of Medical Sciences, New Delhi, India

    Krishna Kant, Anil Kumar Tomar & Savita Yadav

  2. Department of Laboratory Medicine, All India Institute of Medical Sciences, New Delhi, India

    Sarman Singh

Authors
  1. Krishna Kant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anil Kumar Tomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarman Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Savita Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Savita Yadav.

Ethics declarations

Conflict of interest

Authors of this manuscript declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 301 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kant, K., Tomar, A.K., Singh, S. et al. Ageing associated proteomic variations in seminal plasma of Indian men. J Proteins Proteom 10, 83–89 (2019). https://doi.org/10.1007/s42485-019-00013-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42485-019-00013-x

Keywords

Search

Navigation