Membrane stability and mitochondrial activity of human-ejaculated spermatozoa during in vitro experimental infection with Escherichia coli, Staphylococcus haemolyticus and Bacteroides ureolyticus

Andrologia

Volumn 44, Issue 5, 2012, Pages 315-329

  Fraczek, M ^a   Piasecka, M ^b   Gaczarzewicz, D ^c   Szumala Kakol, A ^d   Kazienko, A ^b   Lenart, S ^c   Laszczynska, M ^b   Kurpisz, M ^a  

^a INSTITUTE OF HUMAN GENETICS   (Poland)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

^c WEST POMERANIAN UNIVERSITY OF TECHNOLOGY   (Poland)

^d POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

Mitochondria; Semen infection; Sperm membrane architecture

Indexed keywords

MEROCYANINE;

ARTICLE; BACTERIAL STRAIN; BACTEROIDES; BACTEROIDES INFECTION; BACTEROIDES UREOLYTICUS; BACTEROIDES UREOLYTICUS INFECTION; CELL ACTIVITY; CONTROLLED STUDY; EJACULATION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MALE FERTILITY; MEMBRANE STABILIZATION; MITOCHONDRIAL ACTIVITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; SPERMATOZOON; SPERMATOZOON MOTILITY; STAPHYLOCOCCUS HAEMOLYTICUS; STAPHYLOCOCCUS HAEMOLYTICUS INFECTION; STAPHYLOCOCCUS INFECTION;

ADULT; BACTEROIDES INFECTIONS; BENZIMIDAZOLES; CARBOCYANINES; CELL MEMBRANE; CELL SURVIVAL; ESCHERICHIA COLI INFECTIONS; HUMANS; INFERTILITY, MALE; MALE; MITOCHONDRIA; PYRIMIDINONES; SPERMATOZOA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS HAEMOLYTICUS;

EID: 84865802584     PISSN: 03034569     EISSN: 14390272     Source Type: Journal    
DOI: 10.1111/j.1439-0272.2012.01283.x     Document Type: Article

References (70)

1. Aitken RJ, De Iuliis GN (2010) On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod 16:3-13.
2. Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA (2007) Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 9:554-564.
3. Aprikian P, Tchesnokova V, Kidd B, Yakovenko O, Yarov-Yarovoy V, Trinchina E, Vogel V, Thomas W, Sokurenko E (2007) Interdomain interaction in the FimH adhesin of Escherichia coli regulates the affinity to mannose. J Biol Chem 282:23437-23446.
4. Balmelli T, Stamm J, Dolina-Giudici M, Peduzzi R, Piffaretti-Yanez A, Balerna M (1994) Bacteroides ureolyticus in men consulting for infertility. Andrologia 26:35-38.
5. Barroso G, Taylor S, Morshedi M, Manzur F, Gaviño F, Oehninger S (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.
6. Berktas M, Aydin S, Yilmaz Y, Cecen K, Bozkurt H (2008) Sperm motility changes after coincubation with various uropathogenic microorganisms: an in vitro experimental study. Int Urol Nephrol 40:383-389.
7. Bhomkar P, Materi W, Semenchenko V, Wishart DS (2010) Transcriptional response of E. coli upon FimH-mediated fimbrial adhesion. Gene Regul Syst Bio 4:1-17.
8. Burrello N, Salmeri M, Perdichizzi A, Bellanca S, Pettinato G, D'Agata R, Vicari E, Calogero A (2009) Candida albicans experimental infection: effects on human sperm motility, mitochondrial membrane potential and apoptosis. Reprod Biomed Online 18:496-501.
9. Collodel G, Baccetti B, Capitani S, Moretti E (2005) Necrosis in human spermatozoa. I. Ultrastructural features and FISH study in semen from patients with uro-genital infections. J Submicrosc Cytol Pathol 37:67-73.
10. Comhaire FH, Mahmoud AM, Depuydt CE, Zalata AA, Christophe AB (1999) Mechanisms and effects of male genital tract infection on sperm quality and fertilizing potential: the andrologist's viewpoint. Hum Reprod Update 5:393-398.
11. Cosci I, Moretti E, Collodel G (2008) Lipid peroxidation in human spermatozoa from men with genitourinary infections. Syst Biol Reprod Med 54:75-83.
12. Cunningham KA, Beagley KW (2008) Male genital tract chlamydial infection: implications for pathology and infertility. Biol Reprod 79:180-189.
13. Diemer T, Weidner W, Mitchelmann HW, Schiefer HG, Rovan E, Mayer F (1996) Influence of Escherichia coli on motility parameters of human spermatozoa in vitro. Int J Androl 19:271-277.
14. Diemer T, Huwe P, Michelmann HW, Mayer F, Schiefer HG, Weidner W (2000) Escherichia coli-induced alterations of human spermatozoa. An electron microscopy analysis. Int J Androl 23:178-186.
15. Diemer T, Huwe P, Ludwig M, Hauck EW, Weidner W (2003a) Urogenital infection and sperm motility. Andrologia 35:283-287.
16. Diemer T, Huwe P, Ludwig M, Schroeder-Printzen I, Michelmann HW, Schiefer HG, Weidner W (2003b) Influence of autogenous leucocytes and Escherichia coli on sperm motility parameters in vitro. Andrologia 35:100-105.
17. Eggert-Kruse W, Rohr G, Ströck W, Pohl S, Schwalbach B, Runnebaum B (1995) Anaerobes in ejaculates of subfertile men. Hum Reprod Update 1:462-478.
18. Endtz AW (1974) A rapid staining method for differentiating granulocytes from germinal cells in Papanicolau-stained semen. Acta Cytol 18:2-7.
19. Esfandiari N, Sharma RK, Saleh RA, Thomas AJ Jr, Agarwal A (2003) Utility of the nitroblue tetrazolium reduction test for assessment of reactive oxygen species production by seminal leukocytes and spermatozoa. J Androl 24:862-870.
20. Espinoza JA, Schulz MA, Sánchez R, Villegas JV (2009) Integrity of mitochondrial membrane potential reflects human sperm quality. Andrologia 41:51-54.
21. Fraczek M, Sanocka D, Kurpisz M (2004) Interaction between leucocytes and human spermatozoa influencing reactive oxygen intermediates release. Int J Androl 27:69-75.
22. Fraczek M, Szumala-Kakol A, Jedrzejczak P, Kamieniczna M, Kurpisz M (2007) Bacteria trigger oxygen radical release and sperm lipid peroxidation in in vitro model of semen inflammation. Fertil Steril 88:1076-1085.
23. Gallegos-Avila G, Ortega-Martinez M, Ramos-Gonzalez B, Tijerina-Menchaca R, Ancer-Rodriguez J, Jaramillo-Rangel G (2009) Ultrastructural findings in semen samples of infertile men infected with Chlamydia trachomatis and mycoplasmas. Fertil Steril 91:915-919.
24. 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.
25. Gdoura R, Kchaou W, Chaari C, Znazen A, Keskes L, Rebai T, Hammami A (2007) Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC Infect Dis 7:129.
26. Henkel R, Maass G, Hajimohammad M, Menkveld R, Stalf T, Villegas J, Sánchez R, Kruger TF, Schill WB (2003) Urogenital inflammation: changes of leucocytes and ROS. Andrologia 35:309-313.
27. Huwe P, Diemer T, Ludwig M, Liu J, Schiefer HG, Weidner W (1998) Influence of different uropathogenic microorganisms on human sperm motility parameters in an in vitro experiment. Andrologia 30:55-59.
28. Jendrossek V, Grassmé H, Mueller I, Lang F, Gulbins E (2001) Pseudomonas aeruginosa-induced apoptosis involves mitochondria and stress-activated protein kinases. Infect Immun 69:2675-2683.
29. Keck C, Gerber-Schäfer C, Clad A, Wilhelm C, Breckwoldt M (1998) Seminal tract infections: impact on male fertility and treatment options. Hum Reprod Update 4:891-903.
30. Köhn FM, Erdmann I, Oeda T, El Mulla KF, Schiefer HG, Schill WB (1998) Influence of urogenital infections on sperm functions. Andrologia 30:73-80.
31. 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.
32. Koppers AJ, Garg ML, Aitken RJ (2010) Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic Biol Med 48:112-119.
33. Kullisaar T, Türk S, Punab M, Korrovits P, Kisand K, Rehema A, Zilmer K, Zilmer M, Mändar R (2008) Oxidative stress in leucocytospermic prostatitis patients: preliminary results. Andrologia 40:161-172.
34. Liu JH, Li HY, Cao ZG, Duan YF, Li Y, Ye ZQ (2002) Influence of several uropathogenic microorganisms on human sperm motility parameters in vitro. Asian J Androl 4:179-182.
35. 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.
36. Marchetti C, Jouy N, Leroy-Martin B, Defossez A, Formstecher P, Marchetti P (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.
37. Martin G, Sabido O, Durand P, 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.
38. Martínez-Pastor F, Fernández-Santos MR, del Olmo E, Domínguez-Rebolledo AE, Esteso MC, Montoro V, Garde JJ (2008) Mitochondrial activity and forward scatter vary in necrotic, apoptotic and membrane-intact spermatozoan subpopulations. Reprod Fertil Dev 20:547-556.
39. Menkveld R, Kruger TF (1998) Sperm morphology and male urogenital infections. Andrologia 30:49-53.
40. Merino G, Carranza-Lira S, Murrieta S, Rodriguez L, Cuevas E, Morán C (1995) Bacterial infection and semen characteristics in infertile men. Arch Androl 35:43-47.
41. Monga M, Roberts JA (1994) Spermagglutination by bacteria: receptor-specific interactions. J Androl 15:151-156.
42. Moretti E, Capitani S, Figura N, Pammolli A, Federico MG, Giannerini V, Collodel G (2009) The presence of bacteria species in semen and sperm quality. J Assist Reprod Genet 26:47-56.
43. Muratori M, Porazzi I, Luconi M, Marchiani S, Forti G, Baldi E (2004) AnnexinV binding and merocyanine staining fail to detect human sperm capacitation. J Androl 25:797-810.
44. Nunez-Calonge R, Caballero P, Redondo C, Baguero F, Martinez-Ferrer F, Meseguer MF (1998) Ureoplasma urealyticum reduces motility and induces membrane alterations in human spermatozoa. Hum Reprod 13:2756-2761.
45. Oborna I, Fingerova H, Novotny J, Brezinova J, Svobodova M, Aziz N (2009) Reactive oxygen species in human semen in relation to leukocyte contamination. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 153:53-57.
46. Ochsendorf FR (1999) Infections in the male genital tract and reactive oxygen species. Hum Reprod Update 5:399-420.
47. Paasch U, Grunewald S, Dathe S, Glander HJ (2004) Mitochondria of human spermatozoa are preferentially susceptible to apoptosis. Ann N Y Acad Sci 1030:403-409.
48. Pellati D, Mylonakis I, Bertoloni G, Fiore C, Andrisani A, Ambrosini G, Armanini D (2008) Genital tract infections and infertility. Eur J Obstet Gynecol Reprod Biol 140:3-11.
49. Piasecka M, Kawiak J (2003) Sperm mitochondria of patients with normal sperm motility and with asthenozoospermia: morphological and functional study. Folia Histochem Cytobiol 41:125-139.
50. Piasecka M, Wenda-Rózewicka L, Ogoński T (2001) Computerized analysis of cytochemical reactions for dehydrogenases and oxygraphic studies as methods to evaluate the function of the mitochondrial sheath in rat spermatozoa. Andrologia 33:1-12.
51. Potts JM, Pasqualotto FF (2003) Seminal oxidative stress in patients with chronic prostatitis. Andrologia 35:304-308.
52. Potts JM, Sharma R, Pasqualotto F, Nelson D, Hall G, Agarwal A (2000) Association of Ureaplasma urealyticum with abnormal reactive oxygen species levels and absence of leukocytospermia. J Urol 163:1775-1778.
53. Qiang H, Jiang MS, Lin JY, He WM (2007) Influence of enterococci on human sperm membrane in vitro. Asian J Androl 9:77-81.
54. Ramya T, Misro MM, Sinha D, Nandan D (2010) Sperm function and seminal oxidative stress as tools to identify sperm pathologies in infertile men. Fertil Steril 93:297-300.
55. Sanocka-Maciejewska D, Ciupińska M, Kurpisz M (2005) Bacterial infection and semen quality. J Reprod Immunol 67:51-56.
56. Segnini A, Camejo MI, Proverbio F (2003) Chlamydia trachomatis and sperm lipid peroxidation in infertile men. Asian J Androl 5:47-49.
57. Schulz M, Sánchez R, Soto L, Risopatrón J, Villegas J (2010) Effect of Escherichia coli and its soluble factors on mitochondrial membrane potential, phosphatidylserine translocation, viability, and motility of human spermatozoa. Fertil Steril 94:619-623.
58. Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851-862.
59. Stovall DW, Bailey LE, Talbert LM (1993) The role of aerobic and anaerobic semen cultures in asymptomatic couples undergoing in vitro fertilization: effect on fertilization and pregnancy rates. Fertil Steril 59:197-201.
60. Tremellen K (2008) Oxidative stress and male infertility - a clinical perspective. Hum Reprod Update 14:243-258.
61. Tunc O, Thompson J, Tremellen K (2010) Development of the NBT assay as a marker of sperm oxidative stress. Int J Androl 33:13-21.
62. Urata K, Narahara H, Tanaka Y, Egashira T, Takayama F, Miyakawa I (2001) Effect of endotoxin-induced reactive oxygen species on sperm motility. Fertil Steril 76:163-166.
63. Villegas J, Schulz M, Soto L, Sanchez R (2005) Bacteria induce expression of apoptosis in human spermatozoa. Apoptosis 10:105-110.
64. Wang A, Fanning L, Anderson DJ, Loughlin KR (1997) Generation of reactive oxygen species by leukocytes and sperm following exposure to urogenital tract infection. Arch Androl 39:11-17.
65. Wang X, Sharma RK, Gupta A, George V, Thomas AJ, Falcone T, Agarwal A (2003) Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil Steril 80:844-850.
66. Weidner W, Krause W, Ludwig M (1999) Relevance of male accessory gland infection for subsequent fertility with special focus on prostatitis. Hum Reprod Update 5:421-432.
67. Wolff H, Panhans A, Stolz W, Meurer M (1993) Adherence of Eschericha coli to sperm: a mannose mediated phenomenon leading to agglutination of sperm and E. coli. Fertil Steril 60:154-158.
68. World Health Organization (1999) WHO Laboratory Manual for the Examination of Human Semen and Sperm-cervical Mucus Interactions, 4th edn. Cambridge University Press, Cambridge, UK.
69. Wu GJ, Chang FW, Lee SS, Cheng YY, Chen CH, Chen IC (2009) Apoptosis-related phenotype of ejaculated spermatozoa in patients with varicocele. Fertil Steril 91:831-837.
70. Yakovenko O, Sharma S, Forero M, Tchesnokova V, Aprikian P, Kidd B, Mach A, Vogel V, Sokurenko E, Thomas WE (2008) FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem 283:11596-11605.