Seminal plasma as a diagnostic fluid for male reproductive system disorders

Nature Reviews Urology

Volumn 11, Issue 5, 2014, Pages 278-288

  Drabovich, Andrei P ^a   Saraon, Punit ^c   Jarvi, Keith ^b   Diamandis, Eleftherios P ^b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA GLOBULIN; BETA GLOBULIN; BIOLOGICAL MARKER; CLUSTERIN; FIBRONECTIN; IMMUNOGLOBULIN; MUCIN 6; PLASMINOGEN ACTIVATOR INHIBITOR 3; PROSTATE SPECIFIC ANTIGEN; PROTEOME; SEMINAL PLASMA PROTEIN;

AZOOSPERMIA; DIAGNOSIS; EPIDIDYMITIS; HUMAN; MALE GENITAL SYSTEM DISEASE; MALE INFERTILITY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROSTATITIS; REVIEW; SEMINAL PLASMA; SERUM; TESTIS CANCER; TISSUE SPECIFICITY; URINALYSIS;

BIOLOGICAL MARKERS; DIAGNOSIS, DIFFERENTIAL; HUMANS; MALE; MALE UROGENITAL DISEASES; PROTEOME; PROTEOMICS; SEMEN;

EID: 84901204200     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2014.74     Document Type: Review

References (140)

1. Krieger, J. N., Ross, S. O. & Riley, D. E. Chronic prostatitis: epidemiology and role of infection. Urology 60, 8-12 (2002).
2. Siegel, R., Naishadham, D. & Jemal, A. Cancer statistics, 2013. CA Cancer J. Clin. 63, 11-30 (2013).
3. Mosher, W. D. Reproductive impairments in the United States, 1965-1982 Demography 22, 415-430 (1985).
4. Rao, A. R., Motiwala, H. G. & Karim, O. M. The discovery of prostate-specific antigen. BJU Int. 101, 5-10 (2008).
5. Laflamme, B. A. & Wolfner, M. F. Identification and function of proteolysis regulators in seminal fluid. Mol. Reprod. Dev. 80, 80-101 (2013).
6. Upadhyay, R. D. et al. Proteomics in reproductive biology: beacon for unraveling the molecular complexities. Biochim. Biophys. Acta 1834, 8-15 (2013).
7. Ferens-Sieczkowska, M., Kowalska, B. & Kratz, E. M. Seminal plasma glycoproteins in male infertility and prostate diseases: is there a chance for glyco-biomarkers? Biomarkers 18, 10-22 (2013).
8. Lenzi, A., Picardo, M., Gandini, L. & Dondero, F. Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum. Reprod. Update 2, 246-256 (1996).
9. Yoshida, K. et al. Physiological roles of semenogelin I and zinc in sperm motility and semen coagulation on ejaculation in humans. Mol. Hum. Reprod. 14, 151-156 (2008).
10. Camejo, M. I. et al. Selenium, copper and zinc in seminal plasma of men with varicocele, relationship with seminal parameters. Biol. Trace Elem. Res. 143, 1247-1254 (2011).
11. Li, H. G., Huang, S. Y., Zhou, H., Liao, A. H. & Xiong, C. L. Quick recovery and characterization of cell-free DNA in seminal plasma of normozoospermia and azoospermia: implications for non-invasive genetic utilities. Asian J. Androl. 11, 703-709 (2009).
12. Wu, W. et al. Seminal plasma microRNAs: potential biomarkers for spermatogenesis status. Mol. Hum. Reprod. 18, 489-497 (2012).
13. Gonzales, G. F. Function of seminal vesicles and their role on male fertility. Asian J. Androl. 3, 251-258 (2001).
14. Mann, T. The biochemistry of semen (eds Peters, R. & Young, F. G.) (Methuen, Wiley, 1954).
15. Mann, T. & Lutwak-Mann, C. Male reproductive function and semen (Springer-Verlag, 1981).
16. Mann, T. Secretory function of the prostate, seminal vesicle and other male accessory organs of reproduction. J. Reprod. Fertil. 37, 179-188 (1974).
17. Gonzales, G. F. & Villena, A. True corrected seminal fructose level: a better marker of the function of seminal vesicles in infertile men. Int. J. Androl. 24, 255-260 (2001).
18. Drake, R. R. et al. Clinical collection and protein properties of expressed prostatic secretions as a source for biomarkers of prostatic disease. J. Proteomics 72, 907-917 (2009).
19. Posner, C. Berl. Klin. Wochenschr. 25, 416 (1888).
20. Gray, S. & Huggins, C. Electrophoretic analysis of human semen. Proc. Soc. Exp. Biol. Med. 50, 351-353 (1942).
21. Ross, V., Moore, D. H. & Miller, E. G. Proteins of human seminal plasma. J. Biol. Chem. 144, 667-677 (1942).
22. Sensabaugh, G. F. Isolation and characterization of a semen-specific protein from human seminal plasma: a potential new marker for semen identification. J. Forensic Sci. 23, 106-115 (1978).
23. Edwards, J. J., Tollaksen, S. L. & Anderson, N. G. Proteins of human semen. I. Two-dimensional mapping of human seminal fluid. Clin. Chem. 27, 1335-1340 (1981).
24. Fung, K. Y., Glode, L. M., Green, S. & Duncan, M. W. A comprehensive characterization of the peptide and protein constituents of human seminal fluid. Prostate 61, 171-181 (2004).
25. Starita-Geribaldi, M. et al. Development of narrow immobilized pH gradients covering one pH unit for human seminal plasma proteomic analysis. Proteomics 3, 1611-1619 (2003).
26. Batruch, I. et al. Analysis of seminal plasma from patients with non-obstructive azoospermia and identification of candidate biomarkers of male infertility. J. Proteome Res. 11, 1503-1511 (2012).
27. Geiger, T., Wehner, A., Schaab, C., Cox, J. & Mann, M. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol. Cell. Proteomics 11, M111.014050 (2012).
28. Liu, M. et al. Scanning of novel cancer/testis proteins by human testis proteomic analysis. Proteomics 13, 1200-1210 (2013).
29. Wang, G. et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J. Proteomics 79, 114-122 (2013).
30. Batruch, I. et al. 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. 10, 941-953 (2011).
31. Kagedan, D. et al. Characterization of the seminal plasma proteome in men with prostatitis by mass spectrometry. Clin. Proteomics 9, 2 (2012).
32. Owen, D. H. & Katz, D. F. A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J. Androl. 26, 459-469 (2005).
33. Robert, M. & Gagnon, C. Sperm motility inhibitor from human seminal plasma: presence of a precursor molecule in seminal vesicle fluid and its molecular processing after ejaculation. Int. J. Androl. 17, 232-240 (1994).
34. Pilch, B. & Mann, M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 7, R40 (2006).
35. Milardi, D. et al. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil. Steril. 97, 67-73.e1 (2012).
36. Wang, J. et al. Proteomic analysis of seminal plasma from asthenozoospermia patients reveals proteins that affect oxidative stress responses and semen quality. Asian J. Androl. 11, 484-491 (2009).
37. Penna, G. et al. Seminal plasma cytokines and chemokines in prostate inflammation: interleukin 8 as a predictive biomarker in chronic prostatitis/chronic pelvic pain syndrome and benign prostatic hyperplasia. Eur. Urol. 51, 524-533 (2007).
38. Rolland, A. D. et al. Identification of genital tract markers in the human seminal plasma using an integrative genomics approach. Hum. Reprod. 28, 199-209 (2012).
39. Drabovich, A. P. & Diamandis, E. P. Combinatorial peptide libraries facilitate development of multiple reaction monitoring assays for low-abundance proteins. J. Proteome Res. 9, 1236-1245 (2010).
40. Drabovich, A. P. et al. Differential diagnosis of azoospermia with proteomic biomarkers ECM1 and TEX101 quantified in seminal plasma. Sci. Transl. Med. 5, 212ra160 (2013).
41. Robertson, S. A., Ingman, W. V., O'Leary, S., Sharkey, D. J. & Tremellen, K. P. Transforming growth factor β-a mediator of immune deviation in seminal plasma. J. Reprod. Immunol. 57, 109-128 (2002).
42. Politch, J. A., Tucker, L., Bowman, F. P. & Anderson, D. J. Concentrations and significance of cytokines and other immunologic factors in semen of healthy fertile men. Hum. Reprod. 22, 2928-2935 (2007).
43. Duncan, M. W. & Thompson, H. S. Proteomics of semen and its constituents. Proteomics Clin. Appl. 1, 861-875 (2007).
44. Tanaka, T. et al. Lipocalin-type prostaglandin D synthase (β-trace) is a newly recognized type of retinoid transporter. J. Biol. Chem. 272, 15789-15795 (1997).
45. Kirchhoff, C., Habben, I., Ivell, R. & Krull, N. A major human epididymis-specific cDNA encodes a protein with sequence homology to extracellular proteinase inhibitors. Biol. Reprod. 45, 350-357 (1991).
46. Lilja, H. A kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein. J. Clin. Invest. 76, 1899-1903 (1985).
47. Tanaka, M. et al. Prostatic acid phosphatase degrades lysophosphatidic acid in seminal plasma. FEBS Lett. 571, 197-204 (2004).
48. Hirai, K., Hussey, H. J., Barber, M. D., Price, S. A. & Tisdale, M. J. Biological evaluation of a lipid-mobilizing factor isolated from the urine of cancer patients. Cancer Res. 58, 2359-2365 (1998).
49. Edstrom Hagerwall, A. M. et al. β-Microseminoprotein endows post coital seminal plasma with potent candidacidal activity by a calcium- and pH-dependent mechanism. PLoS Pathog. 8, e1002625 (2012).
50. Wang, T. J., Rittenhouse, H. G., Wolfert, R. L., Lynne, C. M. & Brackett, N. L. PSA concentrations in seminal plasma. Clin. Chem. 44, 895-896 (1998).
51. Catalona, W. J. et al. Measurement of prostate-specific antigen in serum as a screening test for prostate cancer. N. Engl. J. Med. 324, 1156-1161 (1991).
52. Drabovich, A. P., Jarvi, K. & Diamandis, E. P. Verification of male infertility biomarkers in seminal plasma by multiplex selected reaction monitoring assay. Mol. Cell. Proteomics 10, M110.004127 (2011).
53. Andrade-Rocha, F. T. Assessment of exfoliated prostate cells in semen: relationship with the secretory function of the prostate. Am. J. Clin. Pathol. 128, 788-793 (2007).
54. Andrade-Rocha, F. T. Assessment of increased desquamation of epididymal epithelial cells in semen of men as a predictor of acute epididymitis. Urol. J. 8, 320-322 (2011).
55. Fujihara, Y. et al. Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa. Proc. Natl Acad. Sci. USA 110, 8111-8116 (2013).
56. Olivier, A. J. et al. Isolation and characterization of T cells from semen. J. Immunol. Methods 375, 223-231 (2012).
57. Martinez-Prado, E. & Camejo Bermudez, M. I. Expression of IL-6, IL-8, TNF-α, IL-10, HSP-60, anti-HSP-60 antibodies, and anti-sperm antibodies, in semen of men with leukocytes and/or bacteria. Am. J. Reprod. Immunol. 63, 233-243 (2010).
58. Ronquist, G. & Brody, I. The prostasome: its secretion and function in man. Biochim. Biophys. Acta 822, 203-218 (1985).
59. Utleg, A. G. et al. Proteomic analysis of human prostasomes. Prostate 56, 150-161 (2003).
60. Sandvig, K. & Llorente, A. Proteomic analysis of microvesicles released by the human prostate cancer cell line PC-3. Mol. Cell. Proteomics 11, M111.012914 (2012).
61. Thimon, V., Frenette, G., Saez, F., Thabet, M. & Sullivan, R. Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum. Reprod. 23, 1698-1707 (2008).
62. Diamandis, E. P. et al. Seminal plasma biochemical markers and their association with semen analysis findings. Urology 53, 596-603 (1999).
63. Cheng, C. Y. & Mruk, D. D. The blood-testis barrier and its implications for male contraception. Pharmacol. Rev. 64, 16-64 (2012).
64. Mital, P., Hinton, B. T. & Dufour, J. M. The blood-testis and blood-epididymis barriers are more than just their tight junctions. Biol. Reprod. 84, 851-858 (2011).
65. Anastasi, E. et al. HE4: a new potential early biomarker for the recurrence of ovarian cancer. Tumour Biol. 31, 113-119 (2010).
66. Chen, Y. T. et al. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl Acad. Sci. USA 94, 1914-1918 (1997).
67. Simpson, A. J., Caballero, O. L., Jungbluth, A., Chen, Y. T. & Old, L. J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 5, 615-625 (2005).
68. Fijak, M. & Meinhardt, A. The testis in immune privilege. Immunol. Rev. 213, 66-81 (2006).
69. Chen, Y. T. et al. Identification of multiple cancer/testis antigens by allogeneic antibody screening of a melanoma cell line library. Proc. Natl Acad. Sci. USA 95, 6919-6923 (1998).
70. Krumholtz, J. S. et al. Prostate-specific antigen cutoff of 2.6 ng/mL for prostate cancer screening is associated with favorable pathologic tumor features. Urology 60, 469-473 (2002).
71. Prassas, I., Chrystoja, C. C., Makawita, S. & Diamandis, E. P. Bioinformatic identification of proteins with tissue-specific expression for biomarker discovery. BMC Med. 10, 39 (2012).
72. Wu, C., Macleod, I. & Su, A. I. BioGPS and MyGene.info: organizing online, gene-centric information. Nucleic Acids Res. 41, D561-D565 (2013).
73. Taylor, B. S. et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 18, 11-22 (2010).
74. Fagerberg, L. et al. Contribution of antibody-based protein profiling to the human Chromosome-centric Proteome Project (C-HPP). J. Proteome Res. 12, 2439-2448 (2013).
75. Kim, Y. et al. Identification of differentially expressed proteins in direct expressed prostatic secretions of men with organ-confined versus extracapsular prostate cancer. Mol. Cell. Proteomics 11, 1870-1884 (2012).
76. Jarow, J. P., Espeland, M. A. & Lipshultz, L. I. Evaluation of the azoospermic patient. J. Urol. 142, 62-65 (1989).
77. McLachlan, R. I., Rajpert-De Meyts, E., Hoei-Hansen, C. E., de Kretser, D. M. & Skakkebaek, N. E. Histological evaluation of the human testis-approaches to optimizing the clinical value of the assessment: mini review. Hum. Reprod. 22, 2-16 (2007).
78. Dohle, G. R., Elzanaty, S. & van Casteren, N. J. Testicular biopsy: clinical practice and interpretation. Asian J. Androl. 14, 88-93 (2012).
79. Carpi, A., Sabanegh, E. & Mechanick, J. Controversies in the management of nonobstructive azoospermia. Fertil. Steril. 91, 963-970 (2009).
80. Muttukrishna, S. et al. Serum anti-Mullerian hormone and inhibin B in disorders of spermatogenesis. Fertil. Steril. 88, 516-518 (2007).
81. Tsametis, C. et al. Dynamic endocrine test of inhibin B and anti-Mullerian hormone in men with non-obstructive azoospermia. Gynecol. Endocrinol. 27, 661-665 (2011).
82. Heshmat, S. M. et al. Seminal plasma lipocalin-type prostaglandin D synthase: a potential new marker for the diagnosis of obstructive azoospermia. J. Urol. 179, 1077-1080 (2008).
83. Coppola, M. A. et al. SpermCheck Fertility, an immunodiagnostic home test that detects normozoospermia and severe oligozoospermia. Hum. Reprod. 25, 853-861 (2010).
84. Klotz, K. L. et al. Clinical and consumer trial performance of a sensitive immunodiagnostic home test that qualitatively detects low concentrations of sperm following vasectomy. J. Urol. 180, 2569-2576 (2008).
85. Barry, M. J. Clinical practice. Prostate-specific-antigen testing for early diagnosis of prostate cancer. N. Engl. J. Med. 344, 1373-1377 (2001).
86. Heijnsdijk, E. A. et al. Quality-of-life effects of prostate-specific antigen screening. N. Engl. J. Med. 367, 595-605 (2012).
87. Diamandis, E. P. Prostate-specific antigen: its usefulness in clinical medicine. Trends Endocrinol. Metab. 9, 310-316 (1998).
88. Lopez-Otin, C. & Diamandis, E. P. Breast and prostate cancer: an analysis of common epidemiological, genetic, and biochemical features. Endocr. Rev. 19, 365-396 (1998).
89. McNaughton-Collins, M. F. & Barry, M. J. One man at a time-resolving the PSA controversy. N. Engl. J. Med. 365, 1951-1953 (2011).
90. Saraon, P. et al. Proteomic profiling of androgen-independent prostate cancer cell lines reveals a role for protein S during the development of high grade and castration-resistant prostate cancer. J. Biol. Chem. 287, 34019-34031 (2012).
91. Grasso, C. S. et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243 (2012).
92. Khan, A. P. et al. Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancer. Mol. Cell. Proteomics 9, 298-312 (2010).
93. Kim, Y. J. et al. EFEMP1 as a novel DNA methylation marker for prostate cancer: array-based DNA methylation and expression profiling. Clin. Cancer Res. 17, 4523-4530 (2011).
94. Tomlins, S. A. et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310, 644-648 (2005).
95. Salami, S. S. et al. Combining urinary detection of TMPRSS2:ERG and PCA3 with serum PSA to predict diagnosis of prostate cancer. Urol. Oncol. 31, 566-571 (2013).
96. Venter, J. C. et al. The sequence of the human genome. Science 291, 1304-1351 (2001).
97. Stenson, P. D. et al. The Human Gene Mutation Database: 2008 update. Genome Med. 1, 13 (2009).
98. Abecasis, G. R. et al. An integrated map of genetic variation from 1, 092 human genomes. Nature 491, 56-65 (2012).
99. Frazer, K. A. et al. A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861 (2007).
100. ENCODE Project Consortium et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
101. Koboldt, D. C. et al. Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70 (2012).
102. Muzny, D. M. et al. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
103. Kosova, G., Scott, N. M., Niederberger, C., Prins, G. S. & Ober, C. Genome-wide association study identifies candidate genes for male fertility traits in humans. Am. J. Hum. Genet. 90, 950-961 (2012).
104. Aston, K. I., Krausz, C., Laface, I., Ruiz-Castane, E. & Carrell, D. T. Evaluation of 172 candidate polymorphisms for association with oligozoospermia or azoospermia in a large cohort of men of European descent. Hum. Reprod. 25, 1383-1397 (2010).
105. Avenarius, M. R. et al. Human male infertility caused by mutations in the CATSPER1 channel protein. Am. J. Hum. Genet. 84, 505-510 (2009).
106. Thomas, G. et al. Multiple loci identified in a genome-wide association study of prostate cancer. Nat. Genet. 40, 310-315 (2008).
107. Eeles, R. A. et al. Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat. Genet. 41, 1116-1121 (2009).
108. Kote-Jarai, Z. et al. Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study. Nat. Genet. 43, 785-791 (2011).
109. Ruark, E. et al. Identification of nine new susceptibility loci for testicular cancer, including variants near DAZL and PRDM14. Nat. Genet. 45, 686-689 (2013).
110. Chung, C. C. et al. Meta-analysis identifies four new loci associated with testicular germ cell tumor. Nat. Genet. 45, 680-685 (2013).
111. Barrett, T. et al. NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res. 39, D1005-D1010 (2011).
112. Kapushesky, M. et al. Gene Expression Atlas update-a value-added database of microarray and sequencing-based functional genomics experiments. Nucleic Acids Res. 40, D1077-D1081 (2012).
113. Legrain, P. et al. The human proteome project: current state and future direction. Mol. Cell. Proteomics 10, M111.009993 (2011).
114. Wang, Q. et al. Mutant proteins as cancer-specific biomarkers. Proc. Natl Acad. Sci. USA 108, 2444-2449 (2011).
115. Kuzmanov, U., Jiang, N., Smith, C. R., Soosaipillai, A. & Diamandis, E. P. Differential N-glycosylation of kallikrein 6 derived from ovarian cancer cells or the central nervous system. Mol. Cell. Proteomics 8, 791-798 (2009).
116. He, J. et al. Antibody-independent targeted quantification of TMPRSS2-ERG fusion protein products in prostate cancer. Mol. Oncol. http://dx.doi.org/10. 1016/j.molonc.2014.02.004.
117. Cima, I. et al. Cancer genetics-guided discovery of serum biomarker signatures for diagnosis and prognosis of prostate cancer. Proc. Natl Acad. Sci. USA 108, 3342-3347 (2011).
118. Huttenhain, R. et al. Reproducible quantification of cancer-associated proteins in body fluids using targeted proteomics. Sci. Transl. Med. 4, 142ra94 (2012).
119. Dellaire, G., Berman, J. N. & Arceci, R. (Eds) Cancer genomics, from bench to personalized medicine (Elsevier, 2014).
120. Vegvari, A. et al. Identification of a novel proteoform of prostate specific antigen (SNP-L132I) in clinical samples by multiple reaction monitoring. Mol. Cell. Proteomics 12, 2761-2773 (2013).
121. Wu, C. et al. Integrated genome and transcriptome sequencing identifies a novel form of hybrid and aggressive prostate cancer. J. Pathol. 227, 53-61 (2012).
122. Saraon, P. et al. Quantitative proteomics reveals that enzymes of the ketogenic pathway are associated with prostate cancer progression. Mol. Cell. Proteomics 12, 1589-1601 (2013).
123. Drabovich, A. P., Pavlou, M. P., Dimitromanolakis, A. & Diamandis, E. P. Quantitative analysis of energy metabolic pathways in MCF-7 breast cancer cells by selected reaction monitoring assay. Mol. Cell. Proteomics 11, 422-434 (2012).
124. Olivetti, L. & Grazioli, L. (Eds) Imaging of urogenital diseases: a color atlas (Springer, 2009).
125. Lawrence, E. M., Gnanapragasam, V. J., Priest, A. N. & Sala, E. The emerging role of diffusion-weighted MRI in prostate cancer management. Nat. Rev. Urol. 9, 94-101 (2012).
126. Picchio, M. et al. The role of choline positron emission tomography/computed tomography in the management of patients with prostate-specific antigen progression after radical treatment of prostate cancer. Eur. Urol. 59, 51-60 (2011).
127. Hirsh, A. Post-coital sperm retrieval could lead to the wider approval of assisted conception by some religions. Hum. Reprod. 11, 245-247 (1996).
128. 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. 28, 858-865 (2007).
129. Drake, R. R. et al. In-depth proteomic analyses of direct expressed prostatic secretions. J. Proteome Res. 9, 2109-2116 (2010).
130. Principe, S. et al. Identification of prostate-enriched proteins by in-depth proteomic analyses of expressed prostatic secretions in urine. J. Proteome Res. 11, 2386-2396 (2012).
131. Ponten, F. et al. A global view of protein expression in human cells, tissues, and organs. Mol. Syst. Biol. 5, 337 (2009).
132. Yang, L., Nyalwidhe, J. O., Guo, S., Drake, R. R. & Semmes, O. J. Targeted identification of metastasis-associated cell-surface sialoglycoproteins in prostate cancer. Mol. Cell. Proteomics 10, M110.007294 (2011).
133. Li, J. et al. Mapping of the human testicular proteome and its relationship with that of the epididymis and spermatozoa. Mol. Cell. Proteomics 10, M110.004630 (2011).
134. Li, J. et al. Systematic mapping and functional analysis of a family of human epididymal secretory sperm-located proteins. Mol. Cell. Proteomics 9, 2517-2528 (2010).
135. Johnston, D. S., Wooters, J., Kopf, G. S., Qiu, Y. & Roberts, K. P. Analysis of the human sperm proteome. Ann. NY Acad. Sci. 1061, 190-202 (2005).
136. Amaral, A. et al. Human sperm tail proteome suggests new endogenous metabolic pathways. Mol. Cell. Proteomics 12, 330-342 (2013).
137. Baker, M. A. et al. Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 13, 61-74 (2013).
138. Litwin, M. S. & Saigal, C. S. in Urologic diseases in America (eds Litwin, M. S. & Saigal, C. S.) 1-738 (US Department of Health and Human Services, Public Health Service, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2007).
139. Feldman, D. R., Bosl, G. J., Sheinfeld, J. & Motzer, R. J. Medical treatment of advanced testicular cancer. JAMA 299, 672-684 (2008).
140. de Mouzon, J. et al. Assisted reproductive technology in Europe, 2007: results generated from European registers by ESHRE. Hum. Reprod. 27, 954-966 (2012).