Not all sperm are equal: Functional mitochondria characterize a subpopulation of human sperm with better fertilization potential

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Sousa, Ana Paula ^a,b   Amaral, Alexandra ^a   Baptista, Marta ^a   Tavares, Renata ^a   Campo, Pedro Caballero ^c   Peregrín, Pedro Caballero ^c   Freitas, Albertina ^d   Paiva, Artur ^d   Almeida Santos, Teresa ^b,e   Ramalho Santos, João ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

^c Human Reproduction Unit   (Spain)

^d Centro de Histocompatibilidade do Centro Coimbra   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; DNA DIRECTED DNA POLYMERASE GAMMA; MITOCHONDRIAL PROTEIN; ALDEHYDE; MITOTRACKER GREEN FM;

ACROSOME; ANIMAL CELL; ARTICLE; CELL SELECTION; CHROMATIN; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; FERTILIZATION; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OOCYTE; PROTEIN EXPRESSION; SEMEN ANALYSIS; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; ANIMAL; CATTLE; CELL FRACTIONATION; CELL SEPARATION; FLOW CYTOMETRY; METABOLISM; METAPHASE; PHYSIOLOGY; SPERMATOZOON; STAINING;

BOVINAE;

ALDEHYDES; ANIMALS; CATTLE; CELL FRACTIONATION; CELL SEPARATION; CHROMATIN; FERTILIZATION; FLOW CYTOMETRY; HUMANS; MALE; METAPHASE; MITOCHONDRIA; OOCYTES; SPERM MOTILITY; SPERMATOZOA; STAINING AND LABELING;

EID: 79952915040     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018112     Document Type: Article

References (59)

1. Holt WV, Van Look KJ, (2004) Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127: 527-535.
2. Holt WV, (2005) Is quality assurance in semen analysis still really necessary? A spermatologist's viewpoint. Hum Reprod 20: 2983-2986.
3. Birkhead TR, (2000) Promiscuity: An Evolutionary History of Sperm Competition and Sexual Conflict: Faber and Faber.
4. Katz DF, Brofeldt BT, Overstreet JW, Hanson FW, (1982) Alteration of cervical mucus by vanguard human spermatozoa. J Reprod Fertil 65: 171-175.
5. Austin CR, (1965) Fertilisation. Foundations of Developmental Biology Series New Jersey Prentice-Hall.
6. Cohen J, Tyler KR, (1980) Sperm populations in the female genital tract of the rabbit. J Reprod Fertil 60: 213-218.
7. Cohen J, McNaughton DC, (1974) Spermatozoa: the probable selection of a small population by the genital tract of the female rabbit. J Reprod Fertil 39: 297-310.
8. Gorus FK, Pipeleers DG, (1981) A rapid method for the fractionation of human spermatozoa according to their progressive motility. Fertil Steril 35: 662-665.
9. Pousette A, Akerlof E, Rosenborg L, Fredricsson B, (1986) Increase in progressive motility and improved morphology of human spermatozoa following their migration through Percoll gradients. Int J Androl 9: 1-13.
10. Henkel RR, Schill WB, (2003) Sperm preparation for ART. Reprod Biol Endocrinol 1: 108.
11. Marchetti C, Obert G, Deffosez A, Formstecher P, 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.
12. Ricci G, Perticarari S, Boscolo R, Montico M, Guaschino S, et al. (2009) Semen preparation methods and sperm apoptosis: swim-up versus gradient-density centrifugation technique. Fertil Steril 91: 632-638.
13. Buffone MG, Doncel GF, Marin Briggiler CI, Vazquez-Levin MH, Calamera JC, (2004) Human sperm subpopulations: relationship between functional quality and protein tyrosine phosphorylation. Hum Reprod 19: 139-146.
14. Chantler E, Abraham-Peskir J, Roberts C, (2004) Consistent presence of two normally distributed sperm subpopulations within normozoospermic human semen: a kinematic study. Int J Androl 27: 350-359.
15. Buffone MG, Verstraeten SV, Calamera JC, Doncel GF, (2009) High cholesterol content and decreased membrane fluidity in human spermatozoa are associated with protein tyrosine phosphorylation and functional deficiencies. J Androl 30: 552-558.
16. Donnelly ET, O'Connell M, McClure N, Lewis SE, (2000) Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. Hum Reprod 15: 1552-1561.
17. Barroso G, Taylor S, Morshedi M, Manzur F, Gavino F, et al. (2006) Mitochondrial membrane potential integrity and plasma membrane translocation of phosphatidylserine as early apoptotic markers: a comparison of two different sperm subpopulations. Fertil Steril 85: 149-154.
18. Sakkas D, Manicardi GC, Tomlinson M, Mandrioli M, Bizzaro D, et al. (2000) The use of two density gradient centrifugation techniques and the swim-up method to separate spermatozoa with chromatin and nuclear DNA anomalies. Hum Reprod 15: 1112-1116.
19. Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, et al. (2001) Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Hum Reprod 16: 2160-2165.
20. Zini A, Mak V, Phang D, Jarvi K, (1999) Potential adverse effect of semen processing on human sperm deoxyribonucleic acid integrity. Fertil Steril 72: 496-499.
21. Zini A, Finelli A, Phang D, Jarvi K, (2000) Influence of semen processing technique on human sperm DNA integrity. Urology 56: 1081-1084.
22. Lopata A, Patullo MJ, Chang A, James B, (1976) A method for collecting motile spermatozoa from human semen. Fertil Steril 27: 677-684.
23. Piomboni P, Bruni E, Capitani S, Gambera L, Moretti E, et al. (2006) Ultrastructural and DNA fragmentation analyses in swim-up selected human sperm. Arch Androl 52: 51-59.
24. Kotwicka M, Filipiak K, Jedrzejczak P, Warchol JB, (2008) Caspase-3 activation and phosphatidylserine membrane translocation in human spermatozoa: is there a relationship? Reprod Biomed Online 16: 657-663.
25. Turner RM, Eriksson RL, Gerton GL, Moss SB, (1999) Relationship between sperm motility and the processing and tyrosine phosphorylation of two human sperm fibrous sheath proteins, pro-hAKAP82 and hAKAP82. Mol Hum Reprod 5: 816-824.
26. Spano M, Cordelli E, Leter G, Lombardo F, Lenzi A, et al. (1999) Nuclear chromatin variations in human spermatozoa undergoing swim-up and cryopreservation evaluated by the flow cytometric sperm chromatin structure assay. Mol Hum Reprod 5: 29-37.
27. Younglai EV, Holt D, Brown P, Jurisicova A, Casper RF, (2001) Sperm swim-up techniques and DNA fragmentation. Hum Reprod 16: 1950-1953.
28. Grunewald S, Paasch U, Glander HJ, (2001) Enrichment of non-apoptotic human spermatozoa after cryopreservation by immunomagnetic cell sorting. Cell Tissue Bank 2: 127-133.
29. Hoogendijk CF, Kruger TF, Bouic PJ, Henkel RR, (2009) A novel approach for the selection of human sperm using annexin V-binding and flow cytometry. Fertil Steril 91: 1285-1292.
30. Dirican EK, Ozgun OD, Akarsu S, Akin KO, Ercan O, et al. (2008) Clinical outcome of magnetic activated cell sorting of non-apoptotic spermatozoa before density gradient centrifugation for assisted reproduction. J Assist Reprod Genet 25: 375-381.
31. Said TM, Grunewald S, Paasch U, Glander HJ, Baumann T, et al. (2005) Advantage of combining magnetic cell separation with sperm preparation techniques. Reprod Biomed Online 10: 740-746.
32. de Vantery Arrighi C, Lucas H, Chardonnens D, de Agostini A, (2009) Removal of spermatozoa with externalized phosphatidylserine from sperm preparation in human assisted medical procreation: effects on viability, motility and mitochondrial membrane potential. Reprod Biol Endocrinol 7: 1.
33. Paasch U, Sharma RK, Gupta AK, Grunewald S, Mascha EJ, et al. (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.
34. Grunewald S, Paasch U, Said TM, Rasch M, Agarwal A, et al. (2006) Magnetic-activated cell sorting before cryopreservation preserves mitochondrial integrity in human spermatozoa. Cell Tissue Bank 7: 99-104.
35. Lee TH, Liu CH, Shih YT, Tsao HM, Huang CC, et al. (2010) Magnetic-activated cell sorting for sperm preparation reduces spermatozoa with apoptotic markers and improves the acrosome reaction in couples with unexplained infertility. Hum Reprod 25: 839-846.
36. Said T, Agarwal A, Grunewald S, Rasch M, Baumann T, et al. (2006) Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol Reprod 74: 530-537.
37. Grunewald S, Reinhardt M, Blumenauer V, Said TM, Agarwal A, et al. (2009) Increased sperm chromatin decondensation in selected nonapoptotic spermatozoa of patients with male infertility. Fertil Steril 92: 572-577.
38. Garner DL, (2006) Flow cytometric sexing of mammalian sperm. Theriogenology 65: 943-957.
39. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, et al. (2009) Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15: 553-572.
40. Amaral A, Ramalho-Santos J, St John JC, (2007) The expression of polymerase gamma and mitochondrial transcription factor A and the regulation of mitochondrial DNA content in mature human sperm. Hum Reprod 22: 1585-1596.
41. Amaral A, Ramalho-Santos J, (2010) Assessment of mitochondrial potential: implications for the correct monitoring of human sperm function. Int J Androl 33: e180-186.
42. Auger J, Leonce S, Jouannet P, Ronot X, (1993) Flow cytometric sorting of living, highly motile human spermatozoa based on evaluation of their mitochondrial activity. J Histochem Cytochem 41: 1247-1251.
43. Gallon F, Marchetti C, Jouy N, Marchetti P, (2006) The functionality of mitochondria differentiates human spermatozoa with high and low fertilizing capability. Fertil Steril 86: 1526-1530.
44. Romanato M, Cameo MS, Bertolesi G, Baldini C, Calvo JC, et al. (2003) Heparan sulphate: a putative decondensing agent for human spermatozoa in vivo. Hum Reprod 18: 1868-1873.
45. Romanato M, Julianelli V, Zappi M, Calvo L, Calvo JC, (2008) The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo. Hum Reprod 23: 1145-1150.
46. Sousa AP, Tavares RS, Velez de la Calle JF, Figueiredo H, Almeida V, et al. (2009) Dual use of Diff-Quik-like stains for the simultaneous evaluation of human sperm morphology and chromatin status. Hum Reprod 24: 28-36.
47. Yanagimachi R, Yanagimachi H, Rogers BJ, (1976) The use of zona-free animal ova as a test-system for the assessment of the fertilizing capacity of human spermatozoa. Biol Reprod 15: 471-476.
48. Rybouchkin A, Dozortsev D, de Sutter P, Qian C, Dhont M, (1995) Intracytoplasmic injection of human spermatozoa into mouse oocytes: a useful model to investigate the oocyte-activating capacity and the karyotype of human spermatozoa. Hum Reprod 10: 1130-1135.
49. Sutovsky P, Schatten G, (2000) Paternal contributions to the mammalian zygote: fertilization after sperm-egg fusion. Int Rev Cytol 195: 1-65.
50. Kasai T, Ogawa K, Mizuno K, Nagai S, Uchida Y, et al. (2002) Relationship between sperm mitochondrial membrane potential, sperm motility, and fertility potential. Asian J Androl 4: 97-103.
51. Marchetti C, Jouy N, Leroy-Martin B, Defossez A, Formstecher P, et al. (2004) Comparison of four fluorochromes for the detection of the inner mitochondrial membrane potential in human spermatozoa and their correlation with sperm motility. Hum Reprod 19: 2267-2276.
52. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, et al. (1999) Ubiquitin tag for sperm mitochondria. Nature 402: 371-372.
53. WHO (2010) WHO Laboratory Manual for the Examination and processing of Human Semen. 5th Edition. Geneva WHO Press.
54. Alvarez JG, Storey BT, (1992) Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J Androl 13: 232-241.
55. Ramalho-Santos J, Amaral A, Sousa AP, Rodrigues AS, Martins L, et al. (2007) Probing the structure and function of mammalian sperm using optical and fluorescence microscopy. In: Mendez-Villas A, Diaz J, editors. Modern Research and Educational Topics in Microscopy Badajoz, Spain FORMATEX pp. 394-402.
56. Varum S, Bento C, Sousa AP, Gomes-Santos CS, Henriques P, et al. (2007) Characterization of human sperm populations using conventional parameters, surface ubiquitination, and apoptotic markers. Fertil Steril 87: 572-583.
57. Palermo G, Joris H, Devroey P, Van Steirteghem AC, (1992) Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340: 17-18.
58. Ramalho-Santos J, Amaral A, Brito R, Freitas M, Almeida Santos T, (2004) Simultaneous analysis of cytoskeletal patterns and chromosome positioning in human fertilization failures. Fertil Steril 82: 1654-1659.
59. Perreault SD, Barbee RR, Slott VL, (1988) Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol 125: 181-186.