Reduced sperm telomere length in individuals with varicocele is associated with reduced genomic integrity

Scientific Reports

Volumn 9, Issue 1, 2019, Pages

  Tahamtan, Sahar ^a,b   Tavalaee, Marziyeh ^a   Izadi, Tayebeh ^a   Barikrow, Nooshin ^b   Zakeri, Zahra ^c   Lockshin, Richard A ^c,d   Abbasi, Homayoun ^e   Nasr Esfahani, Mohammad Hosseini ^a,e  

^a ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d ST JOHN'S UNIVERSITY   (United States)

^e ISFAHAN FERTILITY AND INFERTILITY CENTER   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTAMINE;

ADULT; GENETICS; HUMAN; LIPID PEROXIDATION; MALE; MALE INFERTILITY; METABOLISM; SPERMATOZOON; TELOMERE SHORTENING; ULTRASTRUCTURE; VARICOCELE;

ADULT; DNA; HUMANS; INFERTILITY, MALE; LIPID PEROXIDATION; MALE; PROTAMINES; SPERMATOZOA; TELOMERE SHORTENING; VARICOCELE;

EID: 85062880867     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-019-40707-2     Document Type: Article

References (49)

1. Nöske, H. D. & Weidner, W. Varicocele-a historical perspective. World. J. Urol. 17, 151–157 (1999).
2. The influence of varicocele on parameters of fertility in a large group of men presenting to infertility clinics. World Health Organization. Fertil. Steril. 57, 1289–1293 (1992).
3. Miyaoka, R. & Esteves, S. C. A critical appraisal on the role of varicocele in male infertility. Adv. Urol 2012, 597495 (2012).
4. Agarwal, A. & Saleh, R. A. Role of oxidants in male infertility: rationale significance, and treatment. Urol. Clin. North. Am. 29, 817–827 (2002).
5. Nasr-Esfahani, M. H., Abasi, H., Razavi, S., Ashrafi, S. & Tavalaee, M. Varicocelectomy: semen parameters and protamine deficiency. Int. J. Androl 32, 115–122 (2009).
6. Azadi, L. et al. Zaditen (Ketotifen), as mast cell blocker, improves sperm quality, chromatin integrity and pregnancy rate after varicocelectomy. Int. J. Androl. 34, 446–452 (2011).
7. Tavalaee, M. et al. Semen parameters and chromatin packaging in microsurgical varicocelectomy patients. Int. J. Fertil. Steril. 6, 165–174 (2012).
8. Samplaski, M. K., Lo, K. C., Grober, E. D., Zini, A. & Jarvi, K. A. Varicocelectomy to “upgrade” semen quality to allow couples to use less invasive forms of assisted reproductive technology. Fertil. Steril. 108, 609–612 (2017).
9. Nasr-Esfahani, M. H. & Tavalaee, M. Origin and role of DNA damage in varicocele. Int. J. Fertil. Steril 6, 141–146 (2012).
10. Barekat, F. et al. A Preliminary Study: N-acetyl-L-cysteine Improves Semen Quality following Varicocelectomy. Int. J. Fertil. Steril. 10, 120–126 (2016).
11. Janghorban-Laricheh, E. et al. An association between sperm PLCζ levels and varicocele? J. Assist. Reprod. Genet. 33, 1649–1655 (2016).
12. Ni, K., Spiess, A. N., Schuppe, H. C. & Steger, K. The impact of sperm protamine deficiency and sperm DNA damage on human male fertility: a systematic review and meta-analysis. Andrology 4, 789–799 (2016).
13. Navaeian-Kalat, E. et al. High total acrosin activity in varicocele individuals. Andrologia. 1, 634–641 (2012).
14. Durairajanayagam, D., Agarwal, A. & Ong, C. Causes, effects and molecular mechanisms of testicular heat stress. Reprod. Biomed. Online. 30, 14–27 (2015).
15. Micheli, L. et al. Evaluation of enzymatic and non-enzymatic antioxidants in seminal plasma of men with genitourinary infections, varicocele and idiopathic infertility. Andrology. 4, 456–464 (2016).
16. Mostafa, T., Rashed, L. & Taymour, M. Seminal cyclooxygenase relationship with oxidative stress in infertile oligoasthenoteratozoospermic men with varicocele. Andrologia. 48, 137–142 (2016).
17. Longhese, M. P., Anbalagan, S., Martina, M. & Bonetti, D. The role of shelterin in maintaining telomere integrity. Front. Biosci. (Landmark Ed) 1, 1715–1728 (2012).
18. Thilagavathi, J., Venkatesh, S. & Dada, R. Telomere length in reproduction. Andrologia 45, 289–304 (2013).
19. Samassekou, O., Gadji, M., Drouin, R. & Yan, J. Sizing the ends: normal length of human telomeres. Ann. Anat 192, 284–291 (2010).
20. Campbell, P. J. Telomeres and cancer: from crisis to stability to crisis to stability. Cell. 148, 633–635 (2012).
21. Treff, N. R., Su, J., Taylor, D. & Scott, R. T. Jr. Telomere DNA deficiency is associated with development of human embryonic aneuploidy. PLoS. Genet. 7, e1002161 (2011).
22. Keefe, D. L. & Parry, J. P. New approaches to assisted reproductive technologies. Semin. Reprod. Med. 23, 301–308 (2005).
23. Bahreinian, M. et al. DNA hypomethylation predisposes sperm to DNA damage in individuals with varicocele. Syst. Biol. Reprod. Med. 61, 179–186 (2015).
24. Cho, C. L., Esteves, S. C. & Agarwal, A. Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation. Asian. J. Androl. 18, 186–193 (2016).
25. Cariati, F. et al. Investigation of sperm telomere length as a potential marker of paternal genome integrity and semen quality. Reprod. Biomed. Online. 33, 404–411 (2016).
26. Yang, Q. et al. Sperm telomere length is positively associated with the quality of early embryonic development. Hum. Reprod. 30, 1876–1881 (2015).
27. Turner, S. & Hartshorne, G. M. Telomere lengths in human pronuclei, oocytes and spermatozoa. Mol Hum Reprod. 2013 Aug; 1 9(8):510-8. https://doi.org/10.1093/molehr/gat021. Epub 2013 Mar 20.
28. Liu, L., Blasco, M., Trimarchi, J. & Keefe, D. An essential role for functional telomeres in mouse germ cells during fertilization and early development. Dev. Biol. 249, 74–84 (2002).
29. Rodríguez, S. et al. Critically short telomeres are associated with sperm DNA fragmentation. Fertil. Steril. 84, 843–845 (2005).
30. Liu, J. P. & Li, H. Telomerase in the ovary. Reproduction. 140, 215–222 (2010).
31. Rocca, M. S. et al. Sperm telomere length as a parameter of sperm quality in normozoospermic men. Hum. Reprod. 31, 1158–1163 (2016).
32. Garg, H. & Kumar, R. An update on the role of medical treatment including antioxidant therapy in varicocele. Asian. J. Androl. 18, 222–8 (2016).
33. Ni, K. et al. A comprehensive investigation of sperm DNA damage and oxidative stress injury in infertile patients with subclinical, normozoospermic, and astheno/oligozoospermic clinical varicocoele. Andrology. 4, 816–824 (2016).
34. Hosseinpour, E. et al. Sperm ubiquitination and DNA fragmentation in men with occupational exposure and varicocele. Andrologia. 46, 423–429 (2014).
35. Esteves, S. C. et al. Diagnostic accuracy of sperm DNA degradation index (DDSi) as a potential noninvasive biomarker to identify men with varicocele-associated infertility. Int. Urol. Nephrol. 47, 1471–1477 (2015).
36. Cortés-Gutiérrez, E. I. et al. DNA damage in spermatozoa from infertile men with varicocele evaluated by sperm chromatin dispersion and DBD-FISH. Arch. Gynecol. Obstet. 293, 189–196 (2016).
37. García-Calzón, S. et al. GENOI members Dietary total antioxidant capacity is associated with leukocyte telomere lengthin a children and adolescent population. Clin. Nutr. 34, 694–699 (2015).
38. Romeo, C. & Santoro, G. Free radicals in adolescent varicocele testis. Oxid. Med. Cell. Longev 2014, 912878 (2014).
39. Mostafa, T., Rashed, L. A., Zeidan, A. S. & Hosni, A. Glutathione-S-transferase-oxidative stress relationship in the internal spermatic vein blood of infertile men with varicocele. Andrologia 47, 47–51 (2015).
40. Fujisawa, M., Yoshida, S., Matsumoto, O., Kojima, K. & Kamidono, S. Decrease of topoisomerase I activity in the testes of infertile men with varicocele. Arch. Androl. 21, 45–50 (1988).
41. Yoon, S. P. Apurinic/apyrimidinic endonuclease immunoreactivity in germ cells of experimental varicocele-induced rat testes. Acta. Histochem. 115, 887–892 (2013).
42. Lafuente, R. Sperm telomere length in motile sperm selection techniques:A qFISH approach. Andrologia. 50, 1–7 (2017).
43. Dubin, L. & Amelar, R. D. Varicocele size and results of varicocelectomy in selected subfertile men with varicocele. Fertil. Steril. 21, 606–609 (1970).
44. WHO. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. WHO Press, Geneva, Switzerland (2010).
45. Nasr-Esfahani, M. H., Razavi, S. & Mardani, M. Relation between different human sperm nuclear maturity tests and in vitro fertilization. J. Assist. Reprod. Genet 18, 219–225 (2001).
46. Tavalaee, M., Kiani-Esfahani, A. & Nasr-Esfahani, M. H. Relationship between phospholipase C-zeta, semen parameters, and chromatin status. Syst. Biol. Reprod. Med. 63, 259–268 (2017).
47. Aitken, R. J., Wingate, J. K., De Iuliis, G. N. & McLaughlin, E. A. Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Mol. Hum. Reprod. 13, 203–211 (2007).
48. Cawthon, R. M. Telomere measurement by quantitative PCR. Nucleic. Acids. Res. 30, e47 (2002).
49. O’Callaghan, N. J. & Fenech, M. A quantitative PCR method for measuring absolute telomere length. Biol. Proced. Online. 31, 3 (2011).