Investigation on the origin of sperm DNA fragmentation: Role of apoptosis, immaturity and oxidative stress

Molecular Medicine

Volumn 21, Issue , 2015, Pages 109-122

  Muratori, Monica ^a   Tamburrino, Lara ^a   Marchiani, Sara ^a   Cambi, Marta ^a   Olivito, Biagio ^b   Azzari, Chiara ^b   Forti, Gianni ^a   Baldi, Elisabetta ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CASPASE; CASPASE 3; CASPASE 7; CREATINE KINASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); 8-OXO-7-HYDRODEOXYGUANOSINE; DEOXYGUANOSINE;

ADULT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMATURITY; LEUKOCYTE; MALE; MALE GENITAL SYSTEM; MEMBRANE PERMEABILITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SEMEN ANALYSIS; SIGNAL TRANSDUCTION; SPERM; SPERMATOZOON; SPERMATOZOON MOTILITY; ANALOGS AND DERIVATIVES; DNA DAMAGE; GENE EXPRESSION; GENETICS; METABOLISM;

APOPTOSIS; CASPASES; CREATINE KINASE; DEOXYGUANOSINE; DNA DAMAGE; DNA FRAGMENTATION; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; MALE; OXIDATIVE STRESS; SPERMATOZOA;

EID: 84930200616     PISSN: 10761551     EISSN: 15283658     Source Type: Journal    
DOI: 10.2119/molmed.2014.00158     Document Type: Article

References (72)

1. Ahmadi A, Ng SC. (1999) Developmental capacity of damaged spermatozoa. Hum. Reprod. 14:2279–85
2. Singh NP, et al. (1989) Abundant alkali-sensitive sites in DNA of human and mouse sperm. Exp. Cell Res. 184:461–70
3. Gorczyca W, Traganos F, Jesionowska H, 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. 207:202–5
4. Tamburrino L, et al. (2012) Mechanisms and clinical correlates of sperm DNA damage. Asian J. Androl. 14:24–31
5. Morris ID. (2002) Sperm DNA damage and cancer treatment. Int. J. Androl. 25:255–61
6. Rubes J, et al. (2005) Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Hum. Reprod. 20:2776–83
7. Aitken RJ, Baker MA. (2013) Oxidative stress, spermatozoa and leukocytic infiltration: relationships forged by the opposing forces of microbial invasion and the search for perfection. J. Reprod. Immunol. 100:11–9
8. Sakkas D, Manicardi G, Bianchi PG, Bizzaro D, Bianchi U. (1995) Relationship between the presence of endogenous nicks and sperm chromatin packaging in maturing and fertilizing mouse spermatozoa. Biol. Reprod. 52:1149–55
9. Marcon L, Boissonneault G. (2004) Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol. Reprod. 70:910–8
10. Sakkas D, et al. (1999) Origin of DNA damage in ejaculated human spermatozoa. Rev. Reprod. 4:31–7
11. Taylor SL, et al. (2004) Somatic cell apoptosis markers and pathways in human ejaculated sperm: potential utility as indicators of sperm quality. Mol. Hum. Reprod. 10:825–34
12. Mahfouz RZ, et al. (2009) Evaluation of poly(ADP-ribose) polymerase cleavage (cPARP) in ejaculated human sperm fractions after induction of apoptosis. Fertil. Steril. 91:2210–20
13. Aitken RJ, Bronson R, Smith TB, De Iuliis GN. (2013) The source and significance of DNA damage in human spermatozoa; a commentary on diagnostic strategies and straw man fallacies. Mol. Hum. Reprod. 19:475–85
14. Greco E, et al. (2005) Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum. Reprod. 20:226–30
15. Moskovtsev SI, et al. (2010) Testicular spermatozoa have statistically significantly lower DNA damage compared with ejaculated spermatozoa in patients with unsuccessful oral antioxidant treatment. Fertil. Steril. 93:1142–6
16. Sinha K, Das J, Pal PB, Sil PC. (2013) Oxidative stress: the mitochondria-dependent and mitochondria- independent pathways of apoptosis. Arch. Toxicol. 87:1157–80
17. Oliva R. (2006) Protamines and male infertility. Hum. Reprod. Update. 12:417–35
18. Almeida C, Sousa M, Barros A. (2009) Phosphatidylserine translocation in human spermatozoa from impaired spermatogenesis. Reprod. Biomed. Online. 19:770–7
19. Shukla KK, Mahdi AA, Rajender S. (2012) Apoptosis, spermatogenesis and male infertility. Front Biosci. 4:746–54
20. Lotti F, et al. (2012) Semen apoptotic M540 body levels correlate with testis abnormalities: a study in a cohort of infertile subjects. Hum. Reprod. 27:3393–402
21. Wang X, et al. (2003) Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility. Fertil. Steril. 80:531–5
22. Guz J, et al. (2013) Comparison of oxidative stress/DNA damage in semen and blood of fertile and infertile men. PLoS One. 8:e68490
23. Tarozzi N, et al. (2009) Anomalies in sperm chromatin packaging: implications for assisted reproduction techniques. Reprod. Biomed. Online. 18:486–95
24. Sati L, et al. (2008) Double probing of human spermatozoa for persistent histones, surplus cytoplasm, apoptosis and DNA fragmentation. Reprod. Biomed. Online. 16:570–9
25. Marchetti C, Gallego MA, Defossez A, Formstecher P, Marchetti P. (2004) Staining of human sperm with fluorochrome-labeled inhibitor of caspases to detect activated caspases: correlation with apoptosis and sperm parameters. Hum. Reprod. 19:1127–34
26. Said T, et al. (2006) Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol. Reprod. 74:530–7
27. Barroso G, Morshedi M, Oehninger S. (2000) Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum. Reprod. 15:1338–44
28. De Iuliis GN, et al. (2009) DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2’-deoxyguanosine, a marker of oxidative stress. Biol. Reprod. 81:517–24
29. Sakkas D, et al. (2002) Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol. Reprod. 66:1061–7
30. Muratori M, Forti G, Baldi E. (2008) Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling. Cytometry A. 73:785–7
31. Marchiani S, et al. (2007) Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies. Mol. Hum. Reprod. 13:621–31
32. Huszar G, Vigue L. (1993) Incomplete development of human spermatozoa is associated with increased creatine phosphokinase concentration and abnormal head morphology. Mol. Reprod. Dev. 34:292–8
33. Cayli S, Sakkas D, Vigue L, Demir R, Huszar G. (2004) Cellular maturity and apoptosis in human sperm: creatine kinase, caspase-3 and Bcl-XL levels in mature and diminished maturity sperm. Mol. Hum. Reprod. 10:365–72
34. World Health Organization. (2010) Laboratory Manual for the Examination and Processing of Human Semen. WHO Press, Geneva.
35. Mitchell LA, De Iuliis GN, Aitken RJ. (2010) The TUNEL assay consistently underestimates DNA damage in human spermatozoa and is influenced by DNA compaction and cell vitality: development of an improved methodology. Int.J.Androl. 34:2–13
36. Smith TB, et al. (2013) The presence of a truncated base excision repair pathway in human spermatozoa that is mediated by OGG1. J. Cell Sci. 126:1488–97
37. Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, McLachlan RI. (2010) Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum. Reprod. 25:2415–26
38. Marchiani S, et al. (2011) Sumo1-ylation of human spermatozoa and its relationship with semen quality. Int. J. Androl. 34:581–93
39. Muratori M, et al. (2010) Small variations in crucial steps of TUNEL assay coupled to flow cytometry greatly affect measures of sperm DNA fragmentation. J. Androl. 31:336–45
40. Cambi M, et al. (2013) Development of a specific method to evaluate 8-hydroxy, 2-deoxyguanosine in sperm nuclei: relationship with semen quality in a cohort of 94 subjects. Reproduction. 145:227–35
41. Yang L, et al. (2009) Mice deficient in dihydrolipoyl succinyl transferase show increased vulnerability to mitochondrial toxins. Neurobiol. Dis. 36:320–30
42. Marchiani S, et al. (2014) Characterization and sorting of flow cytometric populations in human semen. Andrology. 2:394–401
43. Franken DR, Franken CJ, de la Guerre H, de Villiers A. (1999) Normal sperm morphology and chromatin packaging: comparison between aniline blue and chromomycin A3 staining. Andrologia. 31:361–6
44. Muratori M, et al. (2008) Nuclear staining identifies two populations of human sperm with different DNA fragmentation extent and relationship with semen parameters. Hum. Reprod. 23:1035–43
45. Marchiani S, et al. (2011) Sumo1-ylation of human spermatozoa and its relationship with semen quality. Int. J. Androl. 34:581–93
46. Grunewald S, Sharma R, Paasch U, Glander HJ, Agarwal A. (2009) Impact of caspase activation in human spermatozoa. Microsc. Res. Tech. 72:878–88
47. Agarwal A, et al. (2009) Potential biological role of poly (ADP-ribose) polymerase (PARP) in male gametes. Reprod. Biol. Endocrinol. 7:143
48. Aziz N, Sharma RK, Mahfouz R, Jha R, Agarwal A. (2011) Association of sperm morphology and the sperm deformity index (SDI) with poly (ADP-ribose) polymerase (PARP) cleavage inhibition. Fertil. Steril. 95:2481–4
49. Kemal Duru N, Morshedi M, Oehninger S. (2000) Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa. Fertil. Steril. 74:1200–7
50. Lozano GM, et al. (2009) Relationship between caspase activity and apoptotic markers in human sperm in response to hydrogen peroxide and progesterone. J. Reprod. Dev. 55:615–21
51. Rahman MB, et al. (2012) Oocyte quality determines bovine embryo development after fertilisation with hydrogen peroxide-stressed spermatozoa. Reprod. Fertil. Dev. 24:608–18
52. Aitken RJ, et al. (2012) Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J. Biol. Chem. 287:33048–60
53. Soldani C, Scovassi AI. (2002) Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis. 7:321–8
54. Counis MF, Torriglia A. (2006) Acid DNases and their interest among apoptotic endonucleases. Biochimie. 88:1851–8
55. Shaha C, Tripathi R, Mishra DP. (2010) Male germ cell apoptosis: regulation and biology. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 365:1501–15
56. 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. 93:3199–207
57. Sotolongo B, Huang TT, Isenberger E, Ward WS. (2005) An endogenous nuclease in hamster, mouse, and human spermatozoa cleaves DNA into loop-sized fragments. J. Androl. 26:272–80
58. Boaz SM, Dominguez K, Shaman JA, Ward WS. (2008) Mouse spermatozoa contain a nuclease that is activated by pretreatment with EGTA and subsequent calcium incubation. J. Cell. Biochem. 103:1636–45
59. Oehninger S, et al. (2003) Presence and significance of somatic cell apoptosis markers in human ejaculated spermatozoa. Reprod. Biomed. Online. 7:469–76
60. Sakkas D, et al. (2004) The presence of abnormal spermatozoa in the ejaculate: did apoptosis fail? Hum. Fertil. (Camb). 7:99–103
61. Jakab A, et al. (2003) Efficacy of the swim-up method in eliminating sperm with diminished maturity and aneuploidy. Hum. Reprod. 18:1481–8
62. Grizard G, et al. (2007) In vitro alachlor effects on reactive oxygen species generation, motility patterns and apoptosis markers in human spermatozoa. Reprod. Toxicol. 23:55–62
63. Martínez-Pastor F, et al. (2009) Reactive oxygen species generators affect quality parameters and apoptosis markers differently in red deer spermatozoa. Reproduction. 137:225–35
64. Kang X, et al. (2012) Effects of hepatitis B virus S protein exposure on sperm membrane integrity and functions. PLoS One. 7:e33471
65. Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A. (2006) Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J. Androl. 8:11–29
66. Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. (2007) Increased testicular 8-hydroxy- 2’-deoxyguanosine in patients with varicocele. BJU Int. 100:863–6
67. Morland I, et al. (2002) Human DNA glycosylases of the bacterial Fpg/MutM superfamily: an alternative pathway for the repair of 8-oxoguanine and other oxidation products in DNA. Nucleic Acids Res. 30:4926–36
68. Aitken RJ, Baker MA. (2013) Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int. J. Dev. Biol. 57:265–72
69. Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. (2014) Oxidative stress and male reproductive health. Asian J. Androl. 16:31–8
70. Smith R, Vantman D, Ponce J, Escobar J, Lissi E. (1996) Total antioxidant capacity of human seminal plasma. Hum. Reprod. 11:1655–60
71. Björndahl L, Kvist U. (2010) Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol. Hum. Reprod. 16:23–9
72. Björndahl L, Kvist U. (2014) Structure of Chromatin in Spermatozoa. In: Baldi E and Muratori S, editors. Genetic Damage in Human Spermatozoa. Springer, New York. p 1–11.