Comparative proteomic network signatures in seminal plasma of infertile men as a function of reactive oxygen species

Clinical Proteomics

Volumn 12, Issue 1, 2015, Pages

  Agarwal, Ashok ^a   Ayaz, Ahmet ^a   Samanta, Luna ^a,b   Sharma, Rakesh ^a   Assidi, Mourad ^c   Abuzenadah, Adel M ^c   Sabanegh, Edmund ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b RAVENSHAW UNIVERSITY   (India)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Infertility; Proteome; Reactive oxygen species; Seminal plasma; Sperm function

Indexed keywords

4 TRIMETHYLAMINOBUTYRALDEHYDE DEHYDROGENASE; ADAMTS1 PROTEIN; ALPHA CENTRACTIN; CALNEXIN; CALRETICULIN; CD135 ANTIGEN; CHAPERONE; COL6A2 PROTEIN; CULLIN 3; FAM3D PROTEIN; GLG1 PROTEIN; GLUCOSE REGULATED PROTEIN 94; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUCY1B3 PROTEIN; HADHA PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90 ALPHA; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; MEMBRANE METALLOENDOPEPTIDASE; MMEL1 PROTEIN; NUCB2 PROTEIN; PLASMA PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; SECRETORY PROTEIN; T COMPLEX PROTEIN 1 BETA; T COMPLEX PROTEIN 1 DELTA; T COMPLEX PROTEIN 1 EPSILON; T COMPLEX PROTEIN 1 ZETA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADULT; ARTICLE; BIOINFORMATICS; CHEMOLUMINESCENCE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; DONOR; GEL ELECTROPHORESIS; HUMAN; LIQUID CHROMATOGRAPHY; MALE; MALE FERTILITY; MALE INFERTILITY; MASS SPECTROMETER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEOMICS; SEMEN ANALYSIS; SEMINAL PLASMA; TANDEM MASS SPECTROMETRY;

EID: 84940370235     PISSN: 15426416     EISSN: 15590275     Source Type: Journal    
DOI: 10.1186/s12014-015-9094-5     Document Type: Article

References (72)

1. Robertson SA. Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res. 2005;322:43-52.
2. Fraser LR, Osiguwa OO. Human sperm responses to calcitonin, angiotensin II and fertilization-promoting peptide in prepared semen samples from normal donors and infertility patients. Hum Reprod. 2004;19:596-606.
3. Rando OJ. Daddy issues: paternal effects on phenotype. Cell. 2012;151:702-8.
4. Robertson SA, Seamark RF. Granulocyte macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: stimulation by seminal factors. Reprod Fertil Dev. 1990;2:359-68.
5. Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, et al. Seminal fluid regulates accumulation of FOXP3+ regulatory T cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod. 2011;85:397-408.
6. Robertson SA, Guerin LR, Bromfield JJ, Branson KM, Ahlstrom AC, et al. Seminal fluid drives expansion of the CD4+ CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod. 2009;80:1036-45.
7. Glander HJ, Kratzsch J, Weisbrich C, Birkenmeier G. Insulin-like growth factor-I and alpha 2-macroglobulin in seminal plasma correlate with semen quality. Hum Reprod. 1996;11:2454-60.
8. Wennemuth G, Schiemann PJ, Krause W, Gressner AM, Aumuller G. Influence of fibronectin on the motility of human spermatozoa. Int J Androl. 1997;20:10-6.
9. Irazusta J, Valdivia A, Fernandez D, Agirregoitia E, Ochoa C, et al. Enkephalin-degrading enzymes in normal and subfertile human semen. J Androl. 2004;25:733-9.
10. Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79:829-43.
11. Lavranos G, Balla M, Tzortzopoulou A, Syriou V, Angelopoulou R. Investigating ROS sources in male infertility: a common end for numerous pathways. Reprod Toxicol. 2012;34:298-307.
12. Holmstrom KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol. 2014;15:411-21.
13. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology. 1996;48:835-50.
14. Agarwal A, Sharma RK, Nallella KP, Thomas AJ Jr, Alvarez JG, et al. Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril. 2006;86:878-85.
15. MacLeod Ahmed AH, Allamaneni SS, Comhaire FH, Agarwal A. Relationship between acrosin activity of human spermatozoa and oxidative stress. Asian J Androl. 2004;6:313-8.
16. Aitken RJ, Buckingham D, Harkiss D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil. 1993;97:441-50.
17. Aitken RJ. A free radical theory of male infertility. Reprod Fertil Dev. 1994;6:19-23 discussion 23-14.
18. Pasqualotto FF, Sharma RK, Potts JM, Nelson DR, Thomas AJ, et al. Seminal oxidative stress in patients with chronic prostatitis. Urology. 2000;55:881-5.
19. Shen H, Ong C. Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med. 2000;28:529-36.
20. Deepinder F, Cocuzza M, Agarwal A. Should seminal oxidative stress measurement be offered routinely to men presenting for infertility evaluation? Endocr Pract. 2008;14:484-91.
21. Ko EY, Sabanegh ES Jr, Agarwal A. Male infertility testing: reactive oxygen species and antioxidant capacity. Fertil Steril. 2014;102:1518-27.
22. Tremellen K. Oxidative stress and male infertility-a clinical perspective. Hum Reprod Update. 2008;14:243-58.
23. Wang G, Guo Y, Zhou T, Shi X, Yu J, et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J Proteomics. 2013;79:114-22.
24. Hamada A, Sharma R, du Plessis SS, Willard B, Yadav SP, et al. Two-dimensional differential in-gel electrophoresis-based proteomics of male gametes in relation to oxidative stress. Fertil Steril. 2013;99(1216-1226):e1212.
25. Sharma R, Agarwal A, Mohanty G, Hamada AJ, Gopalan B, et al. Proteomic analysis of human spermatozoa proteins with oxidative stress. Reprod Biol Endocrinol. 2013;11:48.
26. Sharma R, Agarwal A, Mohanty G, Du Plessis SS, Gopalan B, et al. Proteomic analysis of seminal fluid from men exhibiting oxidative stress. Reprod Biol Endocrinol. 2013;11:85.
27. Ayaz A AA, Sharma R, Arafa M, Elbardisi H, Cui Z. Impact of precise modulation of reactive oxygen species levels on spermatozoa proteins in infertile men. Clin Proteomics 2015;12:4.
28. Vernet P, Aitken RJ, Drevet JR. Antioxidant strategies in the epididymis. Mol Cell Endocrinol. 2004;216:31-9.
29. Aitken RJ. Possible redox regulation of sperm motility activation. J Androl. 2000;21:491-6.
30. Rhemrev JP, van Overveld FW, Haenen GR, Teerlink T, Bast A, et al. Quantification of the nonenzymatic fast and slow TRAP in a postaddition assay in human seminal plasma and the antioxidant contributions of various seminal compounds. J Androl. 2000;21:913-20.
31. Ws O, Chen H, Chow PH. Male genital tract antioxidant enzymes-their ability to preserve sperm DNA integrity. Mol Cell Endocrinol. 2006;250:80-3.
32. Organization WH. WHO laboratory manual for the examination and processingof human semen. In: Organization WH, editor. Geneva. Switzerland: WHO Press; 2010.
33. Kashou AH, Sharma R, Agarwal A. Assessment of oxidative stress in sperm and semen. Methods Mol Biol. 2013;927:351-61.
34. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74:5383-92.
35. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75:4646-58.
36. Ashburner M. A biologist's view of the Drosophila genome annotation assessment project. Genome Res. 2000;10:391-3.
37. Gokce E, Shuford CM, Franck WL, Dean RA, Muddiman DC. Evaluation of normalization methods on GeLC-MS/MS label-free spectral counting data to correct for variation during proteomic workflows. J Am Soc Mass Spectrom. 2011;22:2199-208.
38. Blondeau F, Ritter B, Allaire PD, Wasiak S, Girard M, Hussain NK, Angers A, Legendre-Guillemin V, Roy L, Boismenu D, Kearney RE, Bell AW, Bergeron JJ, McPherson PS. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA. 2004;101:3833-8.
39. Powell DW, Weaver CM, Jennings JL, McAfee KJ, He Y, Weil PA, Link AJ. Cluster analysis of mass spectrometry data reveals a novel component of SAGA. Mol Cell Biol. 2004;24:7249-59.
40. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res. 2006;5:2339-47.
41. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. GO:TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004;20:3710-5.
42. Bhatia VN, Perlman DH, Costello CE, McComb ME. Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal Chem. 2009;81:9819-23.
43. Pilch B, Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 2006;7:R40.
44. Drabovich AP, Jarvi K, Diamandis EP. Verification of male infertility biomarkers in seminal plasma by multiplex selected reaction monitoring assay. Mol Cell Proteomics. 2011;10(M110):004127.
45. Sullivan R, Saez F, Girouard J, Frenette G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis. 2005;35:1-10.
46. Frenette G, Lessard C, Madore E, Fortier MA, Sullivan R. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol Reprod. 2003;69:1586-92.
47. Park KH, Kim BJ, Kang J, Nam TS, Lim JM, et al. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 2011;4:ra31.
48. Cross NL, Mahasreshti P. Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch Androl. 1997;39:39-44.
49. Palmerini CA, Saccardi C, Carlini E, Fabiani R, Arienti G. Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction. Fertil Steril. 2003;80:1181-4.
50. Babiker AA, Ronquist G, Nilsson UR, Nilsson B. Transfer of prostasomal CD59 to CD59-deficient red blood cells results in protection against complement-mediated hemolysis. Am J Reprod Immunol. 2002;47:183-92.
51. Kelly RW. Immunosuppressive mechanisms in semen: implications for contraception. Hum Reprod. 1995;10:1686-93.
52. Skibinski G, Kelly RW, Harkiss D, James K. Immunosuppression by human seminal plasma-extracellular organelles (prostasomes) modulate activity of phagocytic cells. Am J Reprod Immunol. 1992;28:97-103.
53. Jones JL, Saraswati S, Block AS, Lichti CF, Mahadevan M, et al. Galectin-3 is associated with prostasomes in human semen. Glycoconj J. 2010;27:227-36.
54. Tarazona R, Delgado E, Guarnizo MC, Roncero RG, Morgado S, et al. Human prostasomes express CD48 and interfere with NK cell function. Immunobiology. 2011;216:41-6.
55. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, et al. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones. 2009;14:105-11.
56. Rupik W, Jasik K, Bembenek J, Widlak W. The expression patterns of heat shock genes and proteins and their role during vertebrate's development. Comp Biochem Physiol A Mol Integr Physiol. 2011;159:349-66.
57. Blobel CP, Wolfsberg TG, Turck CW, Myles DG, Primakoff P, et al. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature. 1992;356:248-52.
58. Bornstein P. Thrombospondins: structure and regulation of expression. Faseb j. 1992;6:3290-9.
59. Kuno K, Matsushima K. ADAMTS-1 protein anchors at the extracellular matrix through the thrombospondin type I motifs and its spacing region. J Biol Chem. 1998;273:13912-7.
60. Shindo T, Kurihara H, Kuno K, Yokoyama H, Wada T, et al. ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest. 2000;105:1345-52.
61. Yokoyama H, Wada T, Kobayashi K, Kuno K, Kurihara H, et al. A disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS)-1 null mutant mice develop renal lesions mimicking obstructive nephropathy. Nephrol Dial Transplant. 2002;17(Suppl 9):39-41.
62. Espey LL, Yoshioka S, Russell DL, Robker RL, Fujii S, et al. Ovarian expression of a disintegrin and metalloproteinase with thrombospondin motifs during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 2000;62:1090-5.
63. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, et al. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA. 2000;97:4689-94.
64. Boerboom D, Russell DL, Richards JS, Sirois J. Regulation of transcripts encoding ADAMTS-1 (a disintegrin and metalloproteinase with thrombospondin-like motifs-1) and progesterone receptor by human chorionic gonadotropin in equine preovulatory follicles. J Mol Endocrinol. 2003;31:473-85.
65. Russell DL, Doyle KM, Ochsner SA, Sandy JD, Richards JS. Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem. 2003;278:42330-9.
66. Miller DJ, Winer MA, Ax RL. Heparin-binding proteins from seminal plasma bind to bovine spermatozoa and modulate capacitation by heparin. Biol Reprod. 1990;42:899-915.
67. Miller DJ, First NL, Ax RL. Isolation and characterization of seminal fluid proteins that bind heparin. Adv Exp Med Biol. 1987;219:597-601.
68. Fernandez D, Valdivia A, Irazusta J, Ochoa C, Casis L. Peptidase activities in human semen. Peptides. 2002;23:461-8.
69. Subiran N, Agirregoitia E, Valdivia A, Ochoa C, Casis L, et al. Expression of enkephalin-degrading enzymes in human semen and implications for sperm motility. Fertil Steril. 2008;89:1571-7.
70. Siems WE, Maul B, Wiesner B, Becker M, Walther T, et al. Effects of kinins on mammalian spermatozoa and the impact of peptidolytic enzymes. Andrologia. 2003;35:44-54.
71. Ravina CG, Seda M, Pinto FM, Orea A, Fernandez-Sanchez M, et al. A role for tachykinins in the regulation of human sperm motility. Hum Reprod. 2007;22:1617-25.
72. Zhu Y, Xu G, Patel A, McLaughlin MM, Silverman C, et al. Cloning, expression, and initial characterization of a novel cytokine-like gene family. Genomics. 2002;80:144-50.