Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Proteome profiling of the sperm maturation milieu in the rhesus monkey (Macaca mulatta) epididymis

Xin Liu A , Shao-Hua Jin B , Xue-Xia Liu A , Wen-Juan Wang C and Fu-Jun Liu A D
+ Author Affiliations
- Author Affiliations

A Central Laboratory, Yantai Yu Huang Ding Hospital/Qingdao University, Yantai 264000, Shandong, P.R. China.

B Clinical Laboratory, Yantai Yu Huang Ding Hospital/Qingdao University, Yantai 264000, Shandong, P.R. China.

C Reproduction Medical Center, Yantai Yu Huang Ding Hospital/Qingdao University, Yantai 264000, Shandong, P.R. China.

D Corresponding author. Email: lfjyt@126.com

Reproduction, Fertility and Development 28(6) 732-741 https://doi.org/10.1071/RD14322
Submitted: 29 August 2014  Accepted: 16 September 2014   Published: 30 October 2014

Abstract

The mammalian spermatozoon acquires its fertilising potential during transit through the epididymis, where it interacts with epididymal luminal fluid proteins (the sperm maturation milieu). In order to highlight the epididymal-specific function of the rhesus monkey (Macaca mulatta) in sperm maturation, two-dimensional gel electrophoresis of epididymal luminal fluid proteins was followed by identification by Matrix-Assisted Laser Desorption/ Ionization Time of Flight Mass Spectrometry (MALDI-TOF/MS) or MALDI-TOF/TOF and revealed over five hundred spots, comprising 198 non-redundant proteins. Some mass spectrometric data were confirmed by western blotting identification. Some common epididymal fluid proteins were identified, such as clusterin, α-1-antitrypsin, malate dehydrogenase, L-lactate dehydrogenase B, α-1-acid glycoprotein 1 and α-mannosidase. More than 7% of all proteins were anti-oxidative, which might control oxidative stress within the male tract. When compared with bull and human epididymal luminal fluid proteins, those in the rhesus monkey had more overlap with the human, which provides evidence of a close evolutionary relationship between the rhesus monkey and man. This study provides new proteomic information on possible rhesus monkey epididymal functions and novel potential biomarkers for the noninvasive assessment of male fertility.

Additional keywords: anti-oxidative, bioinformatics, epididymal fluid, evolution, mass spectrometry.


References

Aitken, R. J., Nixon, B., Lin, M., Koppers, A. J., Lee, Y. H., and Baker, M. A. (2007). Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J. Androl. 9, 554–564.
Proteomic changes in mammalian spermatozoa during epididymal maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptVSlt7s%3D&md5=0e183844a9add6bbf4add872872b88a7CAS | 17589795PubMed |

Bedford, J. M. (1967). Effects of duct ligation on the fertilising ability of spermatozoa from different regions of the rabbit epididymis. J. Exp. Zool. 166, 271–281.
Effects of duct ligation on the fertilising ability of spermatozoa from different regions of the rabbit epididymis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7is1Wksg%3D%3D&md5=30f2eb181a3cbeee06f7a5c68eb650feCAS | 6080554PubMed |

Belleannée, C., Labas, V., Teixeira-Gomes, A. P., Gatti, J. L., Dacheux, J. L., and Dacheux, F. (2011). Identification of luminal and secreted proteins in bull epididymis. J. Proteomics 74, 59–78.
Identification of luminal and secreted proteins in bull epididymis.Crossref | GoogleScholarGoogle Scholar | 20692385PubMed |

Brooks, D. E., and Higgins, S. J. (1980). Characterisation and androgen-dependence of proteins associated with luminal fluid and spermatozoa in the rat epididymis. J. Reprod. Fertil. 59, 363–375.
Characterisation and androgen-dependence of proteins associated with luminal fluid and spermatozoa in the rat epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlsVCqur8%3D&md5=6f8d172e4eefb480e684488e97e2bd18CAS | 7431293PubMed |

Cooper, T. G., and Yeung, C. H. (2010). Physiology of sperm maturation and fertilization. In ‘Andrology: Male Reproductive Health and Dysfunction’. 3rd edn. (Eds E. Nieschlag, H. M. Behre, S. Nieschlag.) pp. 61–85. (Springer: Berlin.)

Dacheux, J. L., Belghazi, M., Lanson, Y., and Dacheux, F. (2006). Human epididymal secretome and proteome. Mol. Cell. Endocrinol. 250, 36–42.
Human epididymal secretome and proteome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVGjtrs%3D&md5=b8f8641cf9e4af7a56d8b2226e94009bCAS | 16431015PubMed |

Dacheux, J. L., Belleannée, C., Jones, R., Labas, V., Belghazi, M., Guyonnet, B., Druart, X., Gatti, J. L., and Dacheux, F. (2009a). Mammalian epididymal proteome. Mol. Cell. Endocrinol. 306, 45–50.
Mammalian epididymal proteome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1ait7Y%3D&md5=3143d313c028da09a1a559b1c824647cCAS | 19464100PubMed |

Dacheux, J. L., Dacheux, F., Labas, V., Ecroyd, H., Nixon, B., and Jones, R. C. (2009b). New proteins identified in epididymal fluid from the platypus (Ornithorhynchus anatinus). Reprod. Fertil. Dev. 21, 1002–1007.
New proteins identified in epididymal fluid from the platypus (Ornithorhynchus anatinus).Crossref | GoogleScholarGoogle Scholar | 19874724PubMed |

Dacheux, J. L., Belleannée, C., Guyonnet, B., Labas, V., Teixeira-Gomes, A. P., Ecroyd, H., Druart, X., Gatti, J. L., and Dacheux, F. (2012). The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Syst. Biol. Reprod. Med 58, 197–210.
The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVemurvL&md5=6849c9829d961ca8be8840cfb8e07588CAS | 22788532PubMed |

Druart, X., Gatti, J. L., Dacheux, F., and Dacheux, J. L. (1994). Analysis by two-dimensional gel electrophoresis of ram epididymal secreted proteins. Cell. Mol. Biol. (Noisy-le-grand) 40, 91–93.
| 1:CAS:528:DyaK2cXjtFylt7Y%3D&md5=4950e5ab45ff8c04e95179242e351164CAS |

Fouchécourt, S., Métayer, S., Locatelli, A., Dacheux, F., and Dacheux, J. L. (2000). Stallion epididymal fluid proteome: qualitative and quantitative characterisation; secretion and dynamic changes of major proteins. Biol. Reprod. 62, 1790–1803.
Stallion epididymal fluid proteome: qualitative and quantitative characterisation; secretion and dynamic changes of major proteins.Crossref | GoogleScholarGoogle Scholar | 10819784PubMed |

Frenette, G., Lessard, C., and Sullivan, R. (2002). Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol. Reprod. 67, 308–313.
Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2iur0%3D&md5=de1479cea256070f4296421dbd030573CAS | 12080033PubMed |

Gibbs, R. A., Rogers, J., Katze, M. G., Bumgarner, R., Weinstock, G. M., Mardis, E. R., Remington, K. A., Strausberg, R. L., Venter, J. C., Wilson, R. K., Batzer, M. A., Bustamante, C. D., Eichler, E. E., Hahn, M. W., Hardison, R. C., Makova, K. D., Miller, W., Milosavljevic, A., Palermo, R. E., Siepel, A., Sikela, J. M., Attaway, T., Bell, S., Bernard, K. E., Buhay, C. J., Chandrabose, M. N., Dao, M., Davis, C., Delehaunty, K. D., Ding, Y., Dinh, H. H., Dugan-Rocha, S., Fulton, L. A., Gabisi, R. A., Garner, T. T., Godfrey, J., Hawes, A. C., Hernandez, J., Hines, S., Holder, M., Hume, J., Jhangiani, S. N., Joshi, V., Khan, Z. M., Kirkness, E. F., Cree, A., Fowler, R. G., Lee, S., Lewis, L. R., Li, Z., Liu, Y. S., Moore, S. M., Muzny, D., Nazareth, L. V., Ngo, D. N., Okwuonu, G. O., Pai, G., Parker, D., Paul, H. A., Pfannkoch, C., Pohl, C. S., Rogers, Y. H., Ruiz, S. J., Sabo, A., Santibanez, J., Schneider, B. W., Smith, S. M., Sodergren, E., Svatek, A. F., Utterback, T. R., Vattathil, S., Warren, W., White, C. S., Chinwalla, A. T., Feng, Y., Halpern, A. L., Hillier, L. W., Huang, X., Minx, P., Nelson, J. O., Pepin, K. H., Qin, X., Sutton, G. G., Venter, E., Walenz, B. P., Wallis, J. W., Worley, K. C., Yang, S. P., Jones, S. M., Marra, M. A., Rocchi, M., Schein, J. E., Baertsch, R., Clarke, L., Csürös, M., Glasscock, J., Harris, R. A., Havlak, P., Jackson, A. R., Jiang, H., Liu, Y., Messina, D. N., Shen, Y., Song, H. X., Wylie, T., Zhang, L., Birney, E., Han, K., Konkel, M. K., Lee, J., Smit, A. F., Ullmer, B., Wang, H., Xing, J., Burhans, R., Cheng, Z., Karro, J. E., Ma, J., Raney, B., She, X., Cox, M. J., Demuth, J. P., Dumas, L. J., Han, S. G., Hopkins, J., Karimpour-Fard, A., Kim, Y. H., Pollack, J. R., Vinar, T., Addo-Quaye, C., Degenhardt, J., Denby, A., Hubisz, M. J., Indap, A., Kosiol, C., Lahn, B. T., Lawson, H. A., Marklein, A., Nielsen, R., Vallender, E. J., Clark, A. G., Ferguson, B., Hernandez, R. D., Hirani, K., Kehrer-Sawatzki, H., Kolb, J., Patil, S., Pu, L. L., Ren, Y., Smith, D. G., Wheeler, D. A., Schenck, I., Ball, E. V., Chen, R., Cooper, D. N., Giardine, B., Hsu, F., Kent, W. J., Lesk, A., Nelson, D. L., O’brien, W. E., Prüfer, K., Stenson, P. D., Wallace, J. C., Ke, H., Liu, X. M., Wang, P., Xiang, A. P., Yang, F., Barber, G. P., Haussler, D., Karolchik, D., Kern, A. D., Kuhn, R. M., Smith, K. E., and Zwieg, A. S. (2007). Evolutionary and biomedical insights from the rhesus macaque genome. Science 316, 222–234.
Evolutionary and biomedical insights from the rhesus macaque genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVeku7Y%3D&md5=afb5c1c446ed11029003f48952e4ca13CAS | 17431167PubMed |

Golan, R., Cooper, T. G., Oschry, Y., Oberpenning, F., Schulze, H., Shochat, L., and Lewin, L. M. (1996). Changes in chromatin condensation of human spermatozoa during epididymal transit as determined by flow cytometry. Hum. Reprod. 11, 1457–1462.
Changes in chromatin condensation of human spermatozoa during epididymal transit as determined by flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28zisVKrug%3D%3D&md5=0effe748b1e9a435fdad2dc9da5c1a28CAS | 8671486PubMed |

Golan, R., Cooper, T. G., Oschry, Y., Weinbauer, G. F., Shochat, L., and Lewin, L. M. (1997). Epididymal maturation of chromatin in spermatozoa from control monkeys (Macaca fascicularis) and those treated with Cetrorelix, a gonadotrophin-releasing hormone antagonist. Biol. Reprod. 57, 354–359.
Epididymal maturation of chromatin in spermatozoa from control monkeys (Macaca fascicularis) and those treated with Cetrorelix, a gonadotrophin-releasing hormone antagonist.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslWgt7o%3D&md5=cd066be7bc7b7ecd7c9b8a61b57a4868CAS | 9241050PubMed |

Görg, A., Weiss, W., and Dunn, M. J. (2004). Current two-dimensional electrophoresis technology for proteomics. Proteomics 4, 3665–3685.
Current two-dimensional electrophoresis technology for proteomics.Crossref | GoogleScholarGoogle Scholar | 15543535PubMed |

Gotham, S. M., Fryer, P. J., and Paterson, W. R. (1988). The measurement of insoluble proteins using a modified Bradford assay. Anal. Biochem. 173, 353–358.
The measurement of insoluble proteins using a modified Bradford assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvVKlt7g%3D&md5=38bb315d14bf6f6a88e82d51a659a3d3CAS | 3189814PubMed |

Grimaldi, G. (2008). The utility of rhesus monkey (Macaca mulatta) and other non-human primate models for preclinical testing of Leishmania candidate vaccines. Mem. Inst. Oswaldo Cruz 103, 629–644.
The utility of rhesus monkey (Macaca mulatta) and other non-human primate models for preclinical testing of Leishmania candidate vaccines.Crossref | GoogleScholarGoogle Scholar |

Li, P., Chan, H. C., He, B., So, S. C., Chung, Y. W., Shang, Q., Zhang, Y. D., and Zhang, Y. L. (2001). An antimicrobial peptide gene found in the male reproductive system of rats. Science 291, 1783–1785.
An antimicrobial peptide gene found in the male reproductive system of rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslSku7g%3D&md5=1ecc51ee4895d60b5fcf752f1e57936fCAS | 11230693PubMed |

Li, J., Liu, F., Wang, H., Liu, X., Liu, J., Li, N., Wan, F., Wang, W., Zhang, C., Jin, S., Liu, J., Zhu, P., and Liu, Y. (2010). Systematic mapping and functional analysis of a family of human epididymal secretory sperm-located proteins. Mol. Cell. Proteomics 9, 2517–2528.
Systematic mapping and functional analysis of a family of human epididymal secretory sperm-located proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFWhs7nM&md5=3239baa0a05ccdf28c5e94128b65eff6CAS | 20736409PubMed |

Liu, Q., Hamil, K. G., Sivashanmugam, P., Grossman, G., Soundararajan, R., Rao, A. J., Richardson, R. T., Zhang, Y. L., O’Rand, M. G., Petrusz, P., French, F. S., and Hall, S. H. (2001). Primate epididymis-specific proteins: characterisation of ESC42, a novel protein containing a trefoil-like motif in monkey and human. Endocrinology 142, 4529–4539.
Primate epididymis-specific proteins: characterisation of ESC42, a novel protein containing a trefoil-like motif in monkey and human.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1erurs%3D&md5=983ad94dff65d3e18ea63c4540c02096CAS | 11564719PubMed |

Liu, X., Wang, W., and Liu, F. (2014). New insight into the castrated mouse epididymis based on comparative proteomics. Reprod. Fertil. Dev , .
New insight into the castrated mouse epididymis based on comparative proteomics.Crossref | GoogleScholarGoogle Scholar | 25209425PubMed |

Nixon, B., Ecroyd, H. W., Dacheux, J. L., and Jones, R. C. (2011). Monotremes provide a key to understanding the evolutionary significance of epididymal sperm maturation. J. Androl. 32, 665–671.
Monotremes provide a key to understanding the evolutionary significance of epididymal sperm maturation.Crossref | GoogleScholarGoogle Scholar | 21441429PubMed |

Orgebin-Crist, M. C. (1967). Fertility in does inseminated with epididymal spermatozoa. J. Reprod. Fertil. 14, 346–347.
Fertility in does inseminated with epididymal spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7it1ensg%3D%3D&md5=eddfe524523e89470ef7588092c3f520CAS | 6079884PubMed |

Sivashanmugam, P., and Rajalakshmi, M. (1997). Sperm maturation in rhesus monkey: changes in ultrastructure, chromatin condensation and organisation of lipid bilayer. Anat. Rec. 247, 25–32.
Sperm maturation in rhesus monkey: changes in ultrastructure, chromatin condensation and organisation of lipid bilayer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsF2iuw%3D%3D&md5=a8e4e16920a3ab02ff7bb6cf769720edCAS | 8986299PubMed |

Skerget, S., Rosenow, M., Polpitiya, A., Petritis, K., Dorus, S., and Karr, T. L. (2013). The Rhesus macaque (Macaca mulatta) sperm proteome. Mol. Cell. Proteomics 12, 3052–3067.
The Rhesus macaque (Macaca mulatta) sperm proteome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWhu7fJ&md5=8a975162e29c5d52f57d0fb8a99ff479CAS | 23816990PubMed |

Srivastav, A., Singh, B., Chandra, A., Jamal, F., Khan, M. Y., and Chowdhury, S. R. (2004). Partial characterisation, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta). Reproduction 127, 343–357.
Partial characterisation, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Ols7s%3D&md5=96ca53213db37ff06b2b2d26a9b6f4ffCAS | 15016954PubMed |

Syntin, P., Dacheux, J. L., and Dacheux, F. (1999). Postnatal development and regulation of proteins secreted in the boar epididymis. Biol. Reprod. 61, 1622–1635.
Postnatal development and regulation of proteins secreted in the boar epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1ynt7o%3D&md5=9ac15d7cfd11e4382c1949917da4a89eCAS | 10570012PubMed |

Thimon, V., Frenette, G., Saez, F., Thabet, M., and Sullivan, R. (2008). Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum. Reprod. 23, 1698–1707.
Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslGqur4%3D&md5=84cac1ac70128189c05133f923c7bff5CAS | 18482993PubMed |

Yeung, C. H., and Cooper, T. G. (2003). Developmental changes in signalling transduction factors in maturing sperm during epididymal transit. Cell. Mol. Biol. (Noisy-le-grand) 49, 341–349.
| 1:CAS:528:DC%2BD3sXls1Krsbc%3D&md5=f7f53ac2440ae5bd5013f4f2a0173d8bCAS |

Yeung, C. H., Cooper, T. G., Oberpenning, F., Schulze, H., and Nieschlag, E. (1993). Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol. Reprod. 49, 274–280.
Changes in movement characteristics of human spermatozoa along the length of the epididymis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3szosFegtA%3D%3D&md5=07a4e569f126afc260943df9dc1b996bCAS | 8373950PubMed |

Yeung, C. H., Cooper, T. G., and Weinbauer, G. F. (1996). Maturation of monkey spermatozoa in the epididymis with respect to their ability to undergo the acrosome reaction. J. Androl. 17, 427–432.
| 1:STN:280:DyaK2s%2FksVKgtw%3D%3D&md5=26e3cb7cd4700127356f90f9adfdb509CAS | 8889706PubMed |

Yeung, C. H., Wang, K., and Cooper, T. G. (2012). Why are epididymal tumours so rare? Asian J. Androl. 14, 465–475.
Why are epididymal tumours so rare?Crossref | GoogleScholarGoogle Scholar | 22522502PubMed |