Proteomic analysis of seminal fluid from men exhibiting oxidative stress

Reproductive Biology and Endocrinology

Volumn 11, Issue 1, 2013, Pages

  Sharma, Rakesh ^a   Agarwal, Ashok ^a   Mohanty, Gayatri ^a,c   Du Plessis, Stefan S ^b   Gopalan, Banu ^a   Willard, Belinda ^a   Yadav, Satya P ^a   Sabanegh, Edmund ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b STELLENBOSCH UNIVERSITY   (South Africa)

^c RAVENSHAW UNIVERSITY   (India)

Author keywords

Differentially expressed proteins; Gene ontology; Male infertility; Mass spectroscopy; Oxidative stress; Proteomics; Reactive oxygen species; Seminal plasma; Varicocele

Indexed keywords

PROLACTIN; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOINFORMATICS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DAMAGE; HUMAN; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROSPECTIVE STUDY; PROTEIN ANALYSIS; PROTEOMICS; SEMINAL PLASMA; TANDEM MASS SPECTROMETRY;

ADULT; ANTIOXIDANTS; BIOLOGICAL MARKERS; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; DNA DAMAGE; HUMANS; INFERTILITY, MALE; MALE; OXIDATIVE STRESS; PROTEOMICS; REACTIVE OXYGEN SPECIES; SEMEN; SEMEN ANALYSIS; TANDEM MASS SPECTROMETRY;

EID: 84883775792     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-11-85     Document Type: Article

References (70)

1. Owen DH, Katz DF. A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J Androl 2005, 26:459-469. 10.2164/jandrol.04104, 15955884.
2. Rolland AD, Lavigne R, Dauly C, Calvel P, Kervarrec C, Freour T, Evrard B, Rioux-Leclercq N, Auger J, Pineau C. Identification of genital tract markers in the human seminal plasma using an integrative genomics approach. Hum Reprod 2013, 28:199-209. 10.1093/humrep/des360, 23024119.
3. Burden HP, Holmes CH, Persad R, Whittington K. Prostasomes-their effects on human male reproduction and fertility. Hum Reprod Update 2006, 12:283-292. 10.1093/humupd/dmi052, 16373403.
4. Kumar V, Hassan MI, Tomar AK, Kashav T, Nautiyal J, Singh S, Singh TP, Yadav S. Proteomic analysis of heparin-binding proteins from human seminal plasma: a step towards identification of molecular markers of male fertility. J Biosci 2009, 34:899-908. 10.1007/s12038-009-0104-5, 20093743.
5. Milardi D, Grande G, Vincenzoni F, Messana I, Pontecorvi A, De Marinis L, Castagnola M, Marana R. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil Steril 2012, 97:67-73. 10.1016/j.fertnstert.2011.10.013, 22088208.
6. Mirza SP, Olivier M. Methods and approaches for the comprehensive characterization and quantification of cellular proteomes using mass spectrometry. Physiol Genomics 2008, 33:3-11. 10.1152/physiolgenomics.00292.2007, 2771641, 18162499.
7. Baker MA, Witherdin R, Hetherington L, Cunningham-Smith K, Aitken RJ. Identification of post-translational modifications that occur during sperm maturation using difference in two-dimensional gel electrophoresis. Proteomics 2005, 5:1003-1012. 10.1002/pmic.200401100, 15712234.
8. Aitken RJ, Baker MA. The role of proteomics in understanding sperm cell biology. Int J Androl 2008, 31:295-302. 10.1111/j.1365-2605.2007.00851.x, 18179557.
9. Steen H, Mann M. The ABC's (and XYZ's) of peptide sequencing. Nat Rev Mol Cell Biol 2004, 5:699-711. 10.1038/nrm1468, 15340378.
10. Syka JE, Coon JJ, Schroeder MJ, Shabanowitz J, Hunt DF. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci U S A 2004, 101:9528-9533. 10.1073/pnas.0402700101, 470779, 15210983.
11. Fung KY, Glode LM, Green S, Duncan MW. A comprehensive characterization of the peptide and protein constituents of human seminal fluid. Prostate 2004, 61:171-181. 10.1002/pros.20089, 15305340.
12. Wang J, Wang J, Zhang HR, Shi HJ, Ma D, Zhao HX, Lin B, Li RS. Proteomic analysis of seminal plasma from asthenozoospermia patients reveals proteins that affect oxidative stress responses and semen quality. Asian J Androl 2009, 11:484-491. 10.1038/aja.2009.26, 19448646.
13. Batruch I, Lecker I, Kagedan D, Smith CR, Mullen BJ, Grober E, Lo KC, Diamandis EP, Jarvi KA. Proteomic analysis of seminal plasma from normal volunteers and post-vasectomy patients identifies over 2000 proteins and candidate biomarkers of the urogenital system. J Proteome Res 2011, 10:941-953. 10.1021/pr100745u, 21142078.
14. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology 1996, 48:835-850. 10.1016/S0090-4295(96)00313-5, 8973665.
15. Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ, Agarwal A. Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril 2000, 73:459-464. 10.1016/S0015-0282(99)00567-1, 10688996.
16. Agarwal A, Sharma RK, Nallella KP, Thomas AJ, Alvarez JG, Sikka SC. Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril 2006, 86:878-885. 10.1016/j.fertnstert.2006.02.111, 17027357.
17. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008, 59:2-11.
18. Tremellen K. Oxidative stress and male infertility--a clinical perspective. Hum Reprod Update 2008, 14:243-258. 10.1093/humupd/dmn004, 18281241.
19. Agarwal A, Sharma RK, Desai NR, Prabakaran S, Tavares A, Sabanegh E. Role of oxidative stress in pathogenesis of varicocele and infertility. Urology 2009, 73:461-469. 10.1016/j.urology.2008.07.053, 19167039.
20. Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A. The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod 1999, 14:2801-2807. 10.1093/humrep/14.11.2801, 10548626.
21. Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod 2011, 26:1628-1640. 10.1093/humrep/der132, 21546386.
22. World Health Organization WHO Laboratory Manual for the Examination and Processing of Human Semen 2010, Geneva, Switzerland, 5, World Health Organization.
23. Benjamin D, Sharma RK, Moazzam A, Agarwal A. Methods for the detection of ROS in human sperm samples. Studies on men's health and fertility 2012, 257-273. New York: Springer Science + Business Media, Agarwal A, Aitken RJ, Alvarez JG.
24. Kashou AH, Sharma R, Agarwal A. Assessment of oxidative stress in sperm and semen. Methods Mol Biol 2013, 927:351-361. 10.1007/978-1-62703-038-0_30, 22992927.
25. Mahfouz R, Sharma R, Sharma D, Sabanegh E, Agarwal A. Diagnostic value of the total antioxidant capacity (TAC) assay in human seminal plasma. Fertil Steril 2009, 91:805-811. 10.1016/j.fertnstert.2008.01.022, 18314108.
26. Sharma RK, Sabanegh E, Mahfouz R, Gupta S, Thiyagarajan A, Agarwal A. TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 2010, 76:1380-1386. 10.1016/j.urology.2010.04.036, 20573380.
27. Sharma R, Agarwal A. Spermatogenesis: an overview. Human sperm chromatin: structure and function. Sperm chromatin. Biological and clinical applications in male infertility and assisted reproduction 2012, 19-44. New York: Springer Science + Business Media, Zini A, Agarwal A.
28. Boyle E, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G. 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, 20:3710-3715. 10.1093/bioinformatics/bth456, 3037731, 15297299.
29. The UniProt Consortium Reorganizing the protein space at the universal protein resource (UniProt). Nucleic Acids Res 2012, 40:D71-D75. 3245120, 22102590, The UniProt Consortium.
30. 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, 81:9819-9823. 10.1021/ac901335x, 2787672, 19839595.
31. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW, Su AI. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 2009, 10:R130. 10.1186/gb-2009-10-11-r130, 3091323, 19919682.
32. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M, Bork P, von Mering C. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009, 37:D412-D416. 10.1093/nar/gkn760, 2686466, 18940858.
33. Michael S, Keiichiro O, Johannes R, Peng-Liang W, Trey I. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27:431-432. 10.1093/bioinformatics/btq675, 3031041, 21149340.
34. Zybailov B, Mosley A, Sardui ME, Coleman MK, Florens L, Washburn MP. Statistical analysis of membrane proteome expressin changes in Saccharomyces cerevisiae. J Prot Res 2006, 5:2339-2347.
35. Liu H, Sadygov RG, Yates JR. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 2004, 76:4193-4201. 10.1021/ac0498563, 15253663.
36. Rodríguez-Martínez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ. Seminal plasma proteins: what role do they play?. Am J Reprod Immunol 2011, 66:11-22.
37. Resing KA, Meyer-Arendt K, Mendoza AM, Aveline-Wolf LD, Jonscher KR, Pierce KG, Old WM, Cheung HT, Russell S, Wattawa JL, et al. Improving reproducibility and sensitivity in identifying human proteins by shotgun proteomics. Anal Chem 2004, 76:3556-3568. 10.1021/ac035229m, 15228325.
38. Katnik-Prastowska I, Przybysz M, Chełmońska-Soyta A. Fibronectin fragments in human seminal plasma. Acta Biochim Pol 2005, 52:557-560.
39. Pinke LA, Swanlund DJ, Hensleigh HC, McCarthy JB, Roberts KP, Pryor JL. Analysis of fibronectin on human sperm. J Urol 1997, 158:936-941. 10.1016/S0022-5347(01)64367-2, 9258122.
40. Davalieva K, Kiprijanovska S, Noveski P, Plaseski T, Kocevska B, Broussard C, Plaseska-Karanfilska D. Proteomic analysis of seminal plasma in men with different spermatogenic impairment. Andrologia 2012, 44:256-264. 10.1111/j.1439-0272.2012.01275.x, 22288839.
41. Eickhoff R, Baldauf C, Koyro HW, Wennemuth G, Suga Y, Seitz J, Henkel R, Meinhardt A. Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Mol Hum Reprod 2004, 10:605-611. 10.1093/molehr/gah075, 15169922.
42. Pacis RA, Pilat MJ, Pienta KJ, Wojno K, Raz A, Hogan V, Cooper CR. Decreased galectin-3 expression in prostate cancer. Prostate 2000, 44:118-1123. 10.1002/1097-0045(20000701)44:2<118::AID-PROS4>3.0.CO;2-U, 10881021.
43. Saraswati S, Block AS, Davidson MK, Rank RG, Mahadevan M, Diekman AB. Galectin-3 is a substrate for prostate specific antigen (PSA) in human seminal plasma. Prostate 2011, 71:197-208. 10.1002/pros.21236, 3606048, 20672323.
44. Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballescà JL, Oliva R. Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 2008, 23:783-791. 10.1093/humrep/den024, 18281682.
45. Bedu-Addo K, Lefièvre L, Moseley FL, Barratt CL, Publicover SJ. Bicarbonate and bovine serum albumin reversibly 'switch' capacitation-induced events in human spermatozoa. Mol Hum Reprod 2005, 11:683-691. 10.1093/molehr/gah226, 16192296.
46. Camargo M, Lopes PI, Del Giudice PT, Carvalho VM, Cardozo KH, Andreoni C, Fraietta R, Bertolla RP. Unbiased label-free quantitative proteomic profiling and enriched proteomic pathways in seminal plasma of adult men before and after varicocelectomy. Hum Reprod 2013, 28:33-46. 10.1093/humrep/des357, 23042794.
47. Kelly RW. Immunosuppressive mechanisms in semen: implications for contraception. Hum Reprod 1995, 10:1686-1693.
48. Autiero M, Bouchier C, Basmaciogullari S, Zaborski P, el Marhomy S, Martin M, Guardiola J, Piatier-Tonneau D. Isolation from a human seminal vesicle library of the cDNA for gp17, a CD4 binding factor. Immunogenetics 1997, 46:345-348.
49. Caputo E, Carratore V, Ciullo M, Tiberio C, Mani JC, Piatier-Tonneau D, Guardiola J. Biosynthesis and immunobiochemical characterization of gp17/GCDFP-15. A glycoprotein from seminal vesicles and from breast tumors, in HeLa cells and in pichia pastoris yeast. Eur J Biochem 1999, 265:664-670. 10.1046/j.1432-1327.1999.00758.x, 10504398.
50. Chiu WW, Chamley LW. Human seminal plasma prolactin-inducible protein is an immunoglobulin G-binding protein. J Reprod Immunol 2003, 60:97-111. 10.1016/S0165-0378(03)00084-6, 14638438.
51. Yamakawa K, Yoshida K, Nishikawa H, Kato T, Iwamoto T. Comparative analysis of interindividual variations in the seminal plasma proteome of fertile men with identification of potential markers for azoospermia in infertile patients. J Androl 2007, 28:858-865. 10.2164/jandrol.107.002824, 17554110.
52. Liao TT, Xiang Z, Zhu WB, Fan LQ. Proteome analysis of round-headed and normal spermatozoa by 2-D fluorescence difference gel electrophoresis and mass spectrometry. Asian J Androl 2009, 1:683-693.
53. Capková J, Elzeinová F, Novák P. Increased expression of secretory actin-binding protein on human spermatozoa is associated with poor semen quality. Hum Reprod 2007, 22:1396-1404. 10.1093/humrep/del511, 17251356.
54. Pilch B, Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 2006, 7:R40. 10.1186/gb-2006-7-5-r40, 1779515, 16709260.
55. Anderson NL, Polanski M, Pieper R, Gatlin T, Tirumalai RS, Conrads TP, Veenstra TD, Adkins JN, Pounds JG, Fagan R, Lobley A. The human plasma proteome: a nonredundant list developed by combination of four separate sources. Mol Cell Proteomics 2004, 3:311-326. 10.1074/mcp.M300127-MCP200, 14718574.
56. Sullivan R, Frenette G, Girouard J. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007, 9:483-491. 10.1111/j.1745-7262.2007.00281.x, 17589785.
57. Barrett AJ, Kirschke H. Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol 1981, 80:535-561.
58. Taugner R, Bührle CP, Nobiling R, Kirschke H. Coexistence of renin and cathepsin B in epithelioid cell secretory granules. Histochemistry 1985, 83:103-108. 10.1007/BF00495138, 3900011.
59. Marks N, Berg MJ, Benuck M. Preferential action of rat brain cathepsin B as a peptidyl dipeptidase converting pro-opioid oligopeptides. Arch Biochem Biophys 1986, 249:489-499. 10.1016/0003-9861(86)90026-3, 3530135.
60. Sloane BF, Honn KV. Cysteine proteinases and metastasis. Cancer Metastasis Rev 1984, 3:249-263. 10.1007/BF00048388, 6093995.
61. Barrett AJ, Davies ME, Grubb A. The place of human gamma-trace (cystatin C) amongst the cysteine proteinase inhibitors. Biochem Biophys Res Commun 1984, 120:631-636. 10.1016/0006-291X(84)91302-0, 6203523.
62. Björck L, Akesson P, Bohus M, Trojnar J, Abrahamson M, Olafsson I, Grubb A. Bacterial growth blocked by a synthetic peptide based on the structure of a human proteinase inhibitor. Nature 1989, 337:385-386. 10.1038/337385a0, 2643059.
63. Block AS, Saraswati S, Lichti CF, Mahadevan M, Diekman AB. Co-purification of Mac-2 binding protein with galectin-3 and association with prostasomes in human semen. Prostate 2011, 71:711-721. 10.1002/pros.21287, 3210485, 21031433.
64. Stanton KJ, Frewin MB, Gudewicz PW. Heterologous desensitization of IL-8-mediated chemotaxis in human neutrophils by a cell-binding fragment of fibronectin. J Leukoc Biol 1999, 65:515-522.
65. Wassarman PM, Litscher ES. Towards the molecular basis of sperm and egg interaction during mammalian fertilization. Cells Tissues Organs 2001, 168:36-45. 10.1159/000016804, 11114585.
66. Jung K, Stephan C, Elgeti U, Lein M, Brux B, Kristiansen G, Rudolph B, Hauptmann S, Schnorr D, Loening SA, Sinha P. Molecular forms of prostate-specific antigen in serum with concentrations of total prostate-specific antigen <4 microg/L: are they useful tools for early detection and screening of prostate cancer?. Int J Cancer 2001, 93:759-765. 10.1002/ijc.1393, 11477592.
67. Ward AM, Catto JW, Hamdy FC. Prostate specific antigen: biology, biochemistry and available commercial assays. Ann Clin Biochem 2001, 38:633-651. 10.1258/0004563011901055, 11732646.
68. Thacker S, Yadav SP, Sharma RK, Kashou A, Willard B, Zhang D, Agarwal A. Evaluation of sperm proteins in infertile men: a proteomic approach. Fertil Steril 2011, 95:2745-2748. 10.1016/j.fertnstert.2011.03.112, 21536282.
69. de Lamirande E, Lamothe G. Levels of semenogelin in human spermatozoa decrease during capacitation: involvement of reactive oxygen species and zinc. Hum Reprod 2010, 25:1619-1630. 10.1093/humrep/deq110, 20501468.
70. Kumar S, Tomar AK, Singh S, Saraswat M, Singh S, Singh TP, Yadav S. Human serum albumin as a new interacting partner of prolactin inducible protein in human seminal plasma. Int J Biol Macromol 2012, 50:317-322. 10.1016/j.ijbiomac.2011.12.015, 22209935.