Critical aspects of detection of sperm DNA fragmentation by tunel/flow cytometry

Systems Biology in Reproductive Medicine

Volumn 56, Issue 4, 2010, Pages 277-285

  Muratori, Monica ^a   Tamburrino, Lara ^a   Marchiani, Sara ^a   Guido, Carmen ^a   Forti, Gianni ^a   Baldi, Elisabetta ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; DNA DAMAGE; DNA FRAGMENTATION; DNA STRAND BREAKAGE; FLOW CYTOMETRY; INTERMETHOD COMPARISON; NICK END LABELING; PRIORITY JOURNAL; REPRODUCIBILITY; REVIEW; SEMEN ANALYSIS;

DNA FRAGMENTATION; FLOW CYTOMETRY; HUMANS; IN SITU NICK-END LABELING; MALE;

EID: 77955883460     PISSN: 19396368     EISSN: 19396368     Source Type: Journal    
DOI: 10.3109/19396368.2010.489660     Document Type: Review

References (70)

1. Alvarez, J. G. (2005) The predictive value of sperm chromatin structure assay. Hum Reprod 20:2365-2367.
2. Aoki, V. W., Emery, B. R., Liu, L. and Carrell, D. T. (2006) Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl 27:890-898.
3. Arpanahi, A., Brinkworth, M., Iles, D., Krawetz, S. A., Paradowska, A., Platts, A. E., et al. (2009) Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 19:1338-1349.
4. Ausubel, M. F., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Strahl, K. (1992) Short Protocols in Molecular Biology, 2nd ed. Greene Publishing Association and John Wiley & Sons, New York, USA.
5. Avendañ o, C., Franchi, A., Duran, H. and Oehninger, S. (2009a) DNA fragmentation of normal spermatozoa negatively impacts embryo quality and intracytoplasmic sperm injection outcome. Fertil Steril. Epub ahead of print.
6. Avendañ o, C., Franchi, A., Taylor, S., Morshedi, M., Bocca, S. and Oehninger, S. (2009b) Fragmentation of DNA in morphologically normal human spermatozoa. Fertil Steril 91:1077-1084.
7. Balhorn, R. (2007) The protamine family of sperm nuclear proteins. Genome Biol 8:227.
8. Bian, Q., Xu, L. C., Wang, S. L., Xia, Y. K., Tan, L. F., Chen, J. F., et al. (2004) Study on the relation between occupational fenvalerate exposure and spermatozoa DNA damage of pesticide factory workers. Occup Environ Med 61:999-1005.
9. Borini, A., Tarozzi, N., Bizzarro, D., Bonu, M. A., Fava, L., Flamini, C. and Coticchio, G. (2006) Sperm DNA fragmentation: paternal effect on early post implantation embryo development in ART. Hum Reprod 21:2876-2881.
10. Brugnon, F., Van Assche, E., Verheyen, G., Sion, B., Boucher, D., Pouly, J. L., et al. (2006) Study of two markers of apoptosis and meiotic segregation in ejaculated sperm of chromosomal translocation carrier patients. Hum Reprod 21:685-693.
11. Caglar, G. S., Köster, F., Schöpper, B., Asimakopoulos, B., Nehls, B., Nikolettos, N., et al. (2007) Semen DNA fragmentation index, evaluated with both TUNEL and Comet assay, and the ICSI outcome. In Vivo 21:1075-1080.
12. Chohan, K. R., Griffin, J. T., Lafromboise, M., De Jonge, C. J. and Carrell, D. T. (2006) Comparison of chromatin assays for DNA fragmentation evaluation in human sperm. J Androl 27:53-59.
13. Cohen-Bacrie, P., Belloc, S., Méné zo, Y. J., Clement, P., Hamidi, J. and Benkhalifa, M. (2009) Correlation between DNA damage and sperm parameters: a prospective study of 1,633 patients. Fertil Steril 91:1801-1805.
14. Derijck, A. A., van der Heijden, G. W., Ramos, L., Giele, M., Kremer, J. A. and de Boer, P. (2007) Motile human normozoospermic and oligozoospermic semen samples show a difference in double-strand DNA break incidence. Hum Reprod 22:2368-2376.
15. Dominguez-Fandos, D., Camejo, M. I., Ballesca', J. L. and Oliva, R. (2007) Human sperm DNA fragmentation: correlation of TUNEL results as assessed by flow cytometry and optical microscopy. Cytometry A 71:1011-1018.
16. Donnelly, E. T., O'Connell, M., McClure, N. and Lewis, S. E. (2000) Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. Hum Reprod 15:1552-1561.
17. Evenson, D. P., Jost, L. K.,Marshall, D., Zinaman,M. J., Clegg, E., Purvis, K., et al. (1999) Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 14:1039-1049.
18. Evenson, D. P., Larson, K. L. and Jost, L. K. (2002) Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23:25-43.
19. Frydman, N., Prisant, N., Hesters, L., Frydman, R., Tachdjian, G., Cohen-Bacrie, P. and Fanchin, R. (2008) Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertil Steril 89:92-97.
20. Genesca, A., Cabalĺn, M. R., Miró , R., Benet, J., Germa, J. R. and Egozcue, J. (1992) Repair of human sperm chromosome aberrations in the hamster egg. Hum Genet 89:181-186.
21. Gold, R., Schmied, M., Giegerich, G., Breitschopf, H., Hartung, H. P., Toyka, K. V. and Lassmann, H. (1994) Differentiation between cellular apoptosis and necrosis by combined use of in situ tailing and nick translation techniques. Lab Invest 71:219-225.
22. Gorczyca, W., Traganos, F., Jesionowska, H. and Darzynkiewicz, Z. (1993) Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res 207:202-205.
23. Greco, E., Romano, S., Iacobelli, M., Ferrero, S., Baroni, E., Minasi, M. G., et al. (2005) ICSI in cases of sperm DNA damage: beneficial effect of oral antioxidant treatment. Hum Reprod 20:2590-2594.
24. Hendzel, M. J. and Bazett-Jones, D. P. (1997) Fixation-dependent organization of core histones following DNA fluorescent in situ hybridization. Chromosoma. 106:114-123.
25. Kamiguchi, Y. and Tateno, H. (2002) Radiation- and chemical-induced structural chromosome aberrations in human spermatozoa. Mutat Res 504:183-191.
26. Kheirollahi-Kouhestani, M., Razavi, S., Tavalaee, M., Deemeh, M. R., Mardani, M., Moshtaghian, J. and Nasr-Esfahani, M. H. (2009) Selection of sperm based on combined density gradient and Zeta method may improve ICSI outcome. Hum Reprod 24:2409-2416.
27. Kozubek, S., Lukásová , E., Amrichová , J., Kozubek, M., Lisková, A. and Slotová , J. (2000) Influence of cell fixation on chromatin topography. Anal Biochem 282:29-38.
28. Lewis, S. E., Agbaje, I. and Alvarez, J. (2008) Sperm DNA tests as useful adjuncts to semen analysis. Syst Biol Reprod Med 54:111-125.
29. Liu, Y., Li, C. M., Lu, Z., Ding, S., Yang, X. and Mo, J. (2006) Studies on formation and repair of formaldehyde-damaged DNA by detection of DNA-protein crosslinks and DNA breaks. Front Biosci 11:991-997.
30. Long, M., Stronati, A., Bizzaro, D., Krüger, T., Manicardi, G. C., Hjelmborg, P. S., Span o, M., Giwercman, A., Toft, G., Bonde, J. P., et al. (2007) Relation between serum xenobiotic-induced receptor activities and sperm DNA damage and sperm apoptotic markers in European and Inuit populations. Reproduction 133:517-530.
31. Manicardi, G. C., Bianchi, P. G., Pantano, S., Azzoni, P., Bizzaro, D., Bianchi, U. and Sakkas, D. (1995) Presence of endogenous nicks in DNA of ejaculated human spermatozoa and its relationship to chromomycin A3 accessibility. Biol Reprod 52:864-867.
32. Manicardi, G. C., Tombacco, A., Bizzaro, D., Bianchi, U., Bianchi, P. G. and Sakkas, D. (1998) DNA strand breaks in ejaculated human spermatozoa: comparison of susceptibility to the nick translation and terminal transferase assays. Histochem J 30:33-39.
33. Marchetti, C., Obert, G., Deffosez, A., Formstecher, P. and Marchetti, P. (2002) Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum Reprod 17:1257-1265.
34. Marchiani, S., Tamburrino, L., Moggi, A., Vannelli, G. B., Forti, G., Baldi, E. and Muratori, M. (2007) Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies. Mol Hum Reprod 13:621-631.
35. Martin, G., Sabido, O., Durand, P. and Levy, R. (2005) Phosphatidylserine externalization in human sperm induced by calcium ionophore A23187: relationship with apoptosis, membrane scrambling and the acrosome reaction. Hum Reprod 20:3459-3468.
36. Muciaccia, B., Corallini, S., Vicini, E., Padula, F., Gandini, L., Liuzzi, G., et al. (2007) HIV-1 viral DNA is present in ejaculated abnormal spermatozoa of seropositive subjects. Hum Reprod 22:2868-2878.
37. Muratori, M., Piomboni, P., Baldi, E., Filimberti, E., Pecchioli, P., Moretti, E., et al. (2000) Functional and ultrastructural features of DNA fragmented human sperm. J Androl 21:903-912.
38. Muratori, M., Forti, G. and Baldi, E. (2008b) Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling. Cytometry A 73:785-787.
39. Muratori, M., Maggi, M., Spinelli, S., Filimberti, E., Forti, G. and Baldi, E. (2003) Spontaneous DNA fragmentation in swim-up selected human spermatozoa during long term incubation. J Androl 24:253-262.
40. Muratori, M., Marchiani, S., Forti, G. and Baldi, E. (2005) Sperm ubiquitination positively correlates to normal morphology in human semen. Hum Reprod 20:1035-1043.
41. Muratori, M., Marchiani, S., Maggi, M., Forti, G. and Baldi, E. (2006) Origin and biological significance of DNA fragmentation in human spermatozoa Front Biosci 11:1491-1499.
42. Muratori, M., Marchiani, S., Tamburrino, L., Tocci, V., Failli, P., Forti, G. and Baldi, E. (2008a) Nuclear staining identifies two populations of human sperm with different DNA fragmentation extent and relationship with semen parameters. Hum Reprod 23:1035-1043.
43. Muratori, M., Tamburrino, L., Tocci, V., Costantino, A., Marchiani, S., Giachini, C., et al. (2009) Small variations in crucial steps of TUNEL assay coupled to flow cytometry greatly affect measures of sperm DNA fragmentation. J Androl (Epub ahead of print).
44. Nakamura, T., Sakai, T. and Hotchi, M. (1995) Histochemical demonstration of DNA double strand breaks by in situ 30-tailing reaction in apoptotic endometrium. Biotech Histochem 70: 33-39.
45. O'Flaherty, C., Vaisheva, F., Hales, B. F., Chan, P. and Robaire, B. (2008) Characterization of sperm chromatin quality in testicular cancer and Hodgkin's lymphoma patients prior to chemotherapy. Hum Reprod 23:1044-1052. (Pubitemid 351757343)
46. Oliva, R. (2006) Protamines and male infertility. Hum Reprod Update 12:417-435.
47. Paasch, U., Sharma, R. K., Gupta, A. K., Grunewald, S., Mascha, E.J, Thomas, A. J. Jr, Glander, H. J. and Agarwal, A. (2004) Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol Reprod 71:1828-1837.
48. Pecou, S., Moinard, N., Walschaerts, M., Pasquier, C., Daudin, M. and Bujan, L. (2009) Ribavirin and pegylated interferon treatment for hepatitis C was associated not only with semen alterations but also with sperm deoxyribonucleic acid fragmentation in humans. Fertil Steril 91:933.e17-933.e22.
49. Piasecka, M., Gaczarzewicz, D., Laszczynska, M., Starczewski, A. and Brodowska, A. (2007) Flow cytometry application in the assessment of sperm DNA integrity of men with asthenozoospermia. Folia Histochem Cytobiol 45(Suppl 1):S127-S136.
50. Ramos, L., van der Heijden, G. W., Derijck, A., Berden, J. H., Kremer, J. A., van der Vlag, J. and de Boer, P. (2008) Incomplete nuclear transformation of human spermatozoa in oligo-astheno-teratospermia: characterization by indirect immunofluorescence of chromatin and thiol status. Hum Reprod 23:259-270.
51. Richardson, C. and Jasin, M. (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 8:697-700.
52. Said, T., Agarwal, A., Grunewald, S., Rasch, M., Baumann, T., Kriegel, C., et al. (2006) Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol Reprod 74:530-537.
53. Schmid, O. and Speit, G. (2007) Genotoxic effects induced by formaldehyde in human blood and implications for the interpretation of biomonitoring studies. Mutagenesis 22:69-74.
54. Sepaniak, S., Forges, T., Gerard, H., Foliguet, B., Bene, M. C. and Monnier-Barbarino, P. (2006) The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 223:54-60.
55. Sergerie, M., Laforest, G., Bujan, L., Bissonnette, F. and Bleau, G. (2005) Sperm DNA fragmentation: threshold value in male fertility. Hum Reprod 20:3446-3451. (Pubitemid 41742526)
56. Sergerie, M., Mieusset, R., Daudin, M., Thonneau, P. and Bujan, L. (2006) Ten-year variation in semen parameters and sperm deoxyribonucleic acid integrity in a healthy fertile man. Fertil Steril 86:1513.e11-18
57. Shaman, J. A. and Ward, W. S. (2006) Sperm chromatin stability and susceptibility to damage in relation to its structure. In: The Sperm Cell: Production, Maturation, Fertilization, Regeneration, De Jonge, C. and Barrat, C. (Eds.), NY: Cambridge University Press; pp. 31-48.
58. Shen, H. and Ong, C. (2000) Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med 28:529-536.
59. Smith, R., Kaune, H., Parodi, D., Madariaga, M., Rios, R., Morales, I. and Castro, A. (2006) Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod 21:986-993.
60. Stronati, A., Manicardi, G. C., Cecati, M., Bordicchia, M., Ferrante, L., Span o, M., et al. (2006) Relationships between sperm DNA fragmentation, sperm apoptotic markers and serum levels of CB-153 and p,p0-DDE in European and Inuit populations. Reproduction 132:949-958.
61. Tarozzi, N., Nadalini, M., Stronati, A., Bizzarro, D., Dal Prato, L., Coticchio, G. and Borini, A. (2009) Anomalies in sperm chromatin packaging: implications for assisted reproduction techniques. Reprod Biomed Online 18:486-495.
62. Tesarik, J., Greco, E. and Mendoza, C. (2004) Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod 19:611-615.
63. Torregrosa, N., Doḿnguez-Fandos, D., Camejo, M. I., Shirley, C. R., Meistrich, M. L., Ballesca, J. L. and Oliva, R. (2006) Protamine 2 precursors, protamine 1/protamine 2 ratio, DNA integrity and other sperm parameters in infertile patients. Hum Reprod 21:2084-2089.
64. Tunc, O., Thompson, J. and Tremellen, K. (2008) Development of the NBT assay as a marker of sperm oxidative stress. Int J Androl (Epub ahead of print).
65. Varum, S., Bento, C., Sousa, A. P., Gomes-Santos, C. S., Henriques, P., Almeida-Santos, T., et al. (2007) Characterization of human sperm populations using conventional parameters, surface ubiquitination, and apoptotic markers. Fertil Steril 87:572-583.
66. Xia, Y., Cheng, S., Bian, Q., Xu, L., Collins, M. D., Chang, H. C., et al. (2005) Genotoxic effects on spermatozoa of carbaryl-exposed workers. Toxicol Sci 85:615-623.
67. Young, K. E., Robbins, W. A., Xun, L., Elashoff, D., Rothmann, S. A. and Perreault, S. D. (2003) Evaluation of chromosome breakage and DNA integrity in sperm: an investigation of remote semen collection conditions. J Androl 24:853-861.
68. Younglai, E. V., Holt, D., Brown, P., Jurisicova, A. and Casper, R. F. (2001) Sperm swim-up techniques and DNA fragmentation. Hum Reprod 16:1950-1953.
69. Zhang, H. B., Lu, S. M., Ma, C. Y., Wang, L., Li, X. and Chen, Z. J. (2008) Early apoptotic changes in human spermatozoa and their relationships with conventional semen parameters and sperm DNA fragmentation. Asian J Androl 10:227-235.
70. Zini, A., Bielecki, R., Phang, D. and Zenzes, M. T. (2001) Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril 75:674-677.