Journal of Reproduction & Infertility

Journal of Reproduction & Infertility

The Challenge of Human Spermatozoa Proteome: A Systematic Review

Authors
Kambiz Gilany 1
Arash Minai-Tehrani 2
Mehdi Amini 3
Niloofar Agharezaee 4
Babak Arjmand 5
1 Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran; Metabolomics and Genomics Research Center, Endocrinology and Metabolism Molecular Cellular Sciences Institute, Tehran University of Medi
2 Nanobiotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran
3 Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran
4 Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran; Department of Genetics, Tehran Medical Sciences Branch, Islamic Azad University, Tehran, Iran
5 Metabolomics and Genomics Research Center, Endocrinology and Metabolism Molecular Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran; Cell Therapy and Regenerative Medicine Research Center, Endocrinol
Abstract
Currently, there are 20,197 human protein-coding genes in the most expertly curated database (UniProtKB/Swiss-Pro). Big efforts have been made by the international consortium, the Chromosome-Centric Human Proteome Project (C-HPP) and independent researchers, to map human proteome. In brief, anno 2017 the human proteome was outlined. The male factor contributes to 50% of infertility in couples. However, there are limited human spermatozoa proteomic studies. Firstly, the development of the mapping of the human spermatozoa was analyzed. The human spermatozoa have been used as a model for missing proteins. It has been shown that human spermatozoa are excellent sources for finding missing proteins. Y chromosome proteome mapping is led by Iran. However, it seems that it is extremely challenging to map the human spermatozoa Y chromosome proteins based on current mass spectrometry-based proteomics technology. Post-translation modifications (PTMs) of human spermatozoa proteome are the most unexplored area and currently the exact role of PTMs in male infertility is unknown. Additionally, the clinical human spermatozoa proteomic analysis, anno 2017 was done in this study.
Keywords
Human
proteome
proteomics
Spermatozoa
Y chromosome
  1. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 2007;35(Database issue):D61-5.
  2. Schlüter H, Apweiler R, Holzhütter HG, Jungblut PR. Finding one's way in proteomics: a protein species nomenclature. Chem Cent J. 2009;3:11.
  3. O'Farrell PH. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975;250(10):4007-21.
  4. Crutchfield CA, Thomas SN, Sokoll LJ, Chan DW. Advances in mass spectrometry-based clinical biomarker discovery. Clin Proteomics. 2016;13:1.
  5. Wilkins MR, Sanchez JC, Gooley AA, Appel RD, Humphery-Smith I, Hochstrasser DF, et al. Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol Genet Eng Rev. 1996;13:19-50.
  6. Bray D. The protein explosion. Nature. 1977;267(5611):481-2.
  7. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature. 2003;422(6928):198-207.
  8. Hondermarck H. Proteomics: biomedical and pharmaceutical applications. 1st ed. Dordrecht: Kluwer Academic Publishers; 2004. 407 p.
  9. Tyers M, Mann M. From genomics to proteomics. Nature. 2003;422(6928):193-7.
  10. Gilany K, Van Elzen R, Mous K, Coen E, Van Dongen W, Vandamme S, et al. The proteome of the human neuroblastoma cell line SH-SY5Y: an enlarged proteome. Biochim Biophys Acta. 2008;1784(7-8):983-5.
  11. Gilany K, Moens L, Dewilde S. Mass spectrometry-based proteomics in the life sciences: a review. J Paramed Sci. 2010;1(1).
  12. Tran JC, Zamdborg L, Ahlf DR, Lee JE, Catherman AD, Durbin KR, et al. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature. 2011;480(7376):254-8.
  13. Chait BT. Chemistry. Mass spectrometry: bottom-up or top-down? Science. 2006;314(5796):65-6.
  14. Smith LM, Kelleher NL; Consortium for Top Down Proteomics. Proteoform: a single term describing protein complexity. Nat Methods. 2013;10(3):186-7.
  15. Patrie SM. Top-down mass spectrometry: proteomics to proteoforms. Adv Exp Med Biol. 2016;919:171-200.
  16. Toby TK, Fornelli L, Kelleher NL. Progress in Top-Down Proteomics and the Analysis of Proteoforms. Annu Rev Anal Chem (Palo Alto Calif). 2016;9(1):499-519.
  17. Cravatt BF, Simon GM, Yates JR 3rd. The biological impact of mass-spectrometry-based proteomics. Nature. 2007;450(7172):991-1000.
  18. Bensimon A, Heck AJ, Aebersold R. Mass spectrometry-based proteomics and network biology. Annu Rev Biochem. 2012;81:379-405.
  19. Legrain P, Aebersold R, Archakov A, Bairoch A, Bala K, Beretta L, et al. The human proteome project: current state and future direction. Mol Cell Proteomics. 2011;10(7):M111.009993.
  20. Paik YK, Jeong SK, Omenn GS, Uhlen M, Hanash S, Cho SY, et al. The chromosome-centric human proteome project for cataloging proteins encoded in the genome. Nat Biotechnol. 2012;30(3):221-3.
  21. Hancock W, Omenn G, Legrain P, Paik YK. Proteomics, human proteome project, and chromosomes. J Proteome Res. 2011;10(1):210.
  22. Paik YK, Omenn GS, Uhlen M, Hanash S, Marko-Varga G, Aebersold R, et al. Standard guidelines for the chromosome-centric human proteome project. J Proteome Res. 2012;11(4):2005-13.
  23. Omenn GS. The strategy, organization, and progress of the HUPO human proteome project. J Proteomics. 2014;100:3-7.
  24. Marko-Varga G, Omenn GS, Paik YK, Hancock WS. A first step toward completion of a genome-wide characterization of the human proteome. J Proteome Res. 2013;12(1):1-5.
  25. Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, Chaerkady R, et al. A draft map of the human proteome. Nature. 2014;509(7502):575-81.
  26. Wilhelm M, Schlegl J, Hahne H, Gholami AM, Lieberenz M, Savitski MM, et al. Mass-spectrometry-based draft of the human proteome. Nature. 2014;509(7502):582-7.
  27. Ezkurdia I, Vázquez J, Valencia A, Tress M. Analyzing the first drafts of the human proteome. J Proteome Res. 2014;13(8):3854-5.
  28. Ezkurdia I, Calvo E, Del Pozo A, Vázquez J, Valencia A, Tress ML. The potential clinical impact of the release of two drafts of the human proteome. Expert Rev Proteomics. 2015;12(6):579-93.
  29. Omenn GS, Lane L, Lundberg EK, Beavis RC, Nesvizhskii AI, Deutsch EW. Metrics for the human proteome project 2015: progress on the human proteome and guidelines for high-confidence protein identification. J Proteome Res. 2015;14(9):3452-60.
  30. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics. tissue-based map of the human proteome. Science. 2015;347(6220):1260419.
  31. Zhang B, Wang J, Wang X, Zhu J, Liu Q, Shi Z, et al. Proteogenomic characterization of human colon and rectal cancer. Nature. 2014;513(7518):382-7.
  32. Hathout Y. Proteomic methods for biomarker discovery and validation. Are we there yet? Expert Rev Proteomics. 2015;12(4):329-31.
  33. Aebersold R, Bader GD, Edwards AM, van Eyk JE, Kussmann M, Qin J, et al. The biology/disease-driven human proteome project (B/D-HPP): enabling protein research for the life sciences community. J Proteome Res. 2013;12(1):23-7.
  34. Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N. Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil. 2015;16(2):61-71.
  35. Kabiri M, Amoozegar MA, Tabebordbar M, Gilany K, Salekdeh GH. Effects of selenite and tellurite on growth, physiology, and proteome of a moderately halophilic bacterium. J Proteome Res. 2009;8(6):3098-108.
  36. Kahn P. From genome to proteome: looking at a cell's proteins. Science. 1995;270(5235):369-70.
  37. Ainsworth C. Cell biology: the secret life of sperm. Nature. 2005;436(7052):770-1.
  38. Baker MA, Reeves G, Hetherington L, Müller J, Baur I, Aitken RJ. Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteomics Clin Appl. 2007;1(5):524-32.
  39. Gilany K, Lakpour N, Vafakhah M, Sadeghi MR. The profile of human sperm proteome; a mini-review. J Reprod Infertil. 2011;12(3):193-9.
  40. Wang G, Guo Y, Zhou T, Shi X, Yu J, Yang Y, et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J Proteomics. 2013;79:114-22.
  41. Amaral A, Castillo J, Ramalho-Santos J, Oliva R. The combined human sperm proteome: cellular pathways and implications for basic and clinical science. Hum Reprod Update. 2014;20(1):40-62.
  42. Johnston DS, Wooters J, Kopf GS, Qiu Y, Roberts KP. Analysis of the human sperm proteome. Ann N Y Acad Sci. 2005;1061:190-202.
  43. de Godoy LM, Olsen JV, de Souza GA, Li G, Mortensen P, Mann M. Status of complete proteome analysis by mass spectrometry: SILAC labeled yeast as a model system. Genome Biol. 2006;7(6):R50.
  44. 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. 2012;11(3):M111.014050.
  45. Breuza L, Poux S, Estreicher A, Famiglietti ML, Magrane M, Tognolli M, et al. The UniProtKB guide to the human proteome. Database (Oxford). 2016;2016.
  46. ProteomicsDB [Internet]. Technische Universität München (TUM) and SAP SE: Germany; 2014 [cited 2017 July 6]. Available from: https://www.proteomicsdb.org/.
  47. Gaudet P, Michel PA, Zahn-Zabal M, Cusin I, Duek PD, Evalet O, et al. The neXtProt knowledgebase on human proteins: current status. Nucleic Acids Res. 2015;43(Database issue):D764-70.
  48. Vogel C, Abreu Rde S, Ko D, Le SY, Shapiro BA, Burns SC, et al. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol. 2010;6:400.
  49. Beck M, Schmidt A, Malmstroem J, Claassen M, Ori A, Szymborska A, et al. The quantitative proteome of a human cell line. Mol Syst Biol. 2011;7:549.
  50. Farrah T, Deutsch EW, Omenn GS, Campbell DS, Sun Z, Bletz JA, et al. A high-confidence human plasma proteome reference set with estimated concentrations in PeptideAtlas. Mol Cell Proteomics. 2011;10(9):M110.006353.
  51. Gaudet P, Argoud-Puy G, Cusin I, Duek P, Evalet O, Gateau A, et al. neXtProt: organizing protein knowledge in the context of human proteome projects. J Proteome Res. 2013;12(1):293-8.
  52. Lane L, Bairoch A, Beavis RC, Deutsch EW, Gaudet P, Lundberg E, et al. Metrics for the human proteome project 2013-2014 and strategies for finding missing proteins. J Proteome Res. 2014;13(1):15-20.
  53. Reddy PJ, Ray S, Srivastava S. The quest of the human proteome and the missing proteins: digging deeper. OMICS. 2015;19(5):276-82.
  54. Fago A, Hundahl C, Dewilde S, Gilany K, Moens L, Weber RE. Allosteric regulation and temperature dependence of oxygen binding in human neuroglobin and cytoglobin. molecular mechanisms and physiological significance. J Biol Chem. 2004;279(43):44417-26.
  55. Horvatovich P, Lundberg EK, Chen YJ, Sung TY, He F, Nice EC, et al. Quest for missing proteins: update 2015 on chromosome-centric human proteome project. J Proteome Res. 2015;14(9):3415-31.
  56. Paik YK, Omenn GS, Overall CM, Deutsch EW, Hancock WS. Recent advances in the chromosome-centric human proteome project: missing proteins in the spot light. J Proteome Res. 2015;14(9):3409-14.
  57. Jumeau F, Com E, Lane L, Duek P, Lagarrigue M, Lavigne R, et al. Human spermatozoa as a model for detecting missing proteins in the context of the chromosome-centric human proteome project. J Proteome Res. 2015;14(9):3606-20.
  58. Hosseini Salekdeh Gh. I-49: Human Y chromosome proteomeproject. Int J Fertil Steril. 2010;4(Suppl 1):49.
  59. Goodfellow P, Darling S, Wolfe J. The human Y chromosome. J Med Genet. 1985;22(5):329-44.
  60. German J, Simpson JL, Chaganti RS, Summitt RL, Reid LB, Merkatz IR. Genetically determined sex-reversal in 46,XY humans. Science. 1978;202(4363):53-6.
  61. Pryor JL, Kent-First M, Muallem A, Van Bergen AH, Nolten WE, Meisner L, et al. Microdeletions in the Y chromosome of infertile men. N Engl J Med. 1997;336(8):534-9.
  62. Cooke HJ. Y chromosome and male infertility. Rev Reprod. 1999;4(1):5-10.
  63. Krausz C, McElreavey K. Y chromosome and male infertility. Front Biosci. 1999;4:E1-8.
  64. Jangravi Z, Alikhani M, Arefnezhad B, Sharifi Tabar M, Taleahmad S, Karamzadeh R, et al. A fresh look at the male-specific region of the human Y chromosome. J Proteome Res. 2013;12(1):6-22.
  65. Rengaraj D, Kwon WS, Pang MG. Bioinformatics annotation of human Y chromosome-encoded protein pathways and interactions. J Proteome Res. 2015;14(9):3503-18.
  66. Gilany K, Aerts M, Dewilde S, Devreese B, Moens L, Vafakhah M. Proteome analysis of mouse brain exposed to chronic hypoxia. Cell. 2011;12(4):503-10.
  67. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447-52.
  68. Croft D, Mundo AF, Haw R, Milacic M, Weiser J, Wu G, et al. The Reactome pathway knowledgebase. Nucleic Acids Res. 2014;42(Database issue):D472-7.
  69. Premkumar E, Bhargava PM. Transcription and translation in bovine spermatozoa. Nat New Biol. 1972;240(100):139-43.
  70. Baker MA. The 'omics revolution and our understanding of sperm cell biology. Asian J Androl. 2011;13(1):6-10.
  71. Zhou T, Xia X, Liu J, Wang G, Guo Y, Guo X, et al. Beyond single modification: reanalysis of the acetylproteome of human sperm reveals widespread multiple modifications. J Proteomics. 2015;126:296-302.
  72. Khoury GA, Baliban RC, Floudas CA. Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database. Sci Rep. 2011;1:90.
  73. Wang G, Wu Y, Zhou T, Guo Y, Zheng B, Wang J, et al. Mapping of the N-linked glycoproteome of human spermatozoa. J Proteome Res. 2013;12(12):5750-9.
  74. Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, et al. Phosphoproteome analysis of capacitated human sperm. evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem. 2003;278(13):11579-89.
  75. Sun G, Jiang M, Zhou T, Guo Y, Cui Y, Guo X, et al. Insights into the lysine acetylproteome of human sperm. J Proteomics. 2014;109:199-211.
  76. World Health Organization, Department of Reproductive Health and Research. WHO laboratory manual for the examination and processing of human semen. 5th ed. Switzerland: World Health Organization; 2010. 286 p.
  77. Oliva R, Castillo J, editors. Sperm nucleoproteins. USA: Springer; 2011. 504 p. (Zini A, Agarwal A, editors. Sperm chromatin: Biological and clinical applications in male infertility and assisted reproduction).
  78. de Mateo S, Martínez-Heredia J, Estanyol JM, Domínguez-Fandos D, Vidal-Taboada JM, Ballescà JL, et al. Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics. 2007;7(23):4264-77.
  79. Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. Oxidative stress and male reproductive health. Asian J Androl. 2014;16(1):31-8.
  80. Hamada A, Sharma R, du Plessis SS, Willard B, Yadav SP, Sabanegh E, et al. Two-dimensional differential in-gel electrophoresis-based proteomics of male gametes in relation to oxidative stress. Fertil Steril. 2013;99(5):1216-26.e2.
  81. Sharma R, Agarwal A, Mohanty G, Hamada AJ, Gopalan B, Willard B, et al. Proteomic analysis of human spermatozoa proteins with oxidative stress. Reprod Biol Endocrinol. 2013;11:48.
  82. Jafarzadeh N, Mani-Varnosfaderani A, Minai-Tehrani A, Savadi-Shiraz E, Sadeghi MR, Gilany K. Metabolomics fingerprinting of seminal plasma from unexplained infertile men: a need for novel diagnostic biomarkers. Mol Reprod Dev. 2015;82(3):150.
  83. Pixton KL, Deeks ED, Flesch FM, Moseley FL, Björndahl L, Ashton PR, et al. Sperm proteome mapping of a patient who experienced failed fertilization at IVF reveals altered expression of at least 20 proteins compared with fertile donors: case report. Hum Reprod. 2004;19(6):1438-47.
  84. Zhao C, Huo R, Wang FQ, Lin M, Zhou ZM, Sha JH. Identification of several proteins involved in regulation of sperm motility by proteomic analysis. Fertil Steril. 2007;87(2):436-8.
  85. 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(4):783-91.
  86. Chan CC, Shui HA, Wu CH, Wang CY, Sun GH, Chen HM, et al. Motility and protein phosphorylation in healthy and asthenozoospermic sperm. J Proteome Res. 2009;8(11):5382-6.
  87. Frapsauce C, Pionneau C, Bouley J, de Larouzière V, Berthaut I, Ravel C, et al. [Unexpected in vitro fertilization failure in patients with normal sperm: a proteomic analysis]. Gynecol Obstet Fertil. 2009;37(10):796-802. French.
  88. 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;11(6):683-93.
  89. Secciani F, Bianchi L, Ermini L, Cianti R, Armini A, La Sala GB, et al. Protein profile of capacitated versus ejaculated human sperm. J Proteome Res. 2009;8(7):3377-89.
  90. Kriegel TM, Heidenreich F, Kettner K, Pursche T, Hoflack B, Grunewald S, et al. Identification of diabetes- and obesity-associated proteomic changes in human spermatozoa by difference gel electrophoresis. Reprod Biomed Online. 2009;19(5):660-70.
  91. Siva AB, Kameshwari DB, Singh V, Pavani K, Sundaram CS, Rangaraj N, et al. Proteomics-based study on asthenozoospermia: differential expression of proteasome alpha complex. Mol Hum Reprod. 2010;16(7):452-62.
  92. Thacker S, Yadav SP, Sharma RK, Kashou A, Willard B, Zhang D, et al. Evaluation of sperm proteins in infertile men: a proteomic approach. Fertil Steril. 2011;95(8):2745-8.
  93. Paasch U, Heidenreich F, Pursche T, Kuhlisch E, Kettner K, Grunewald S, et al. Identification of increased amounts of eppin protein complex components in sperm cells of diabetic and obese individuals by difference gel electrophoresis. Mol Cell Proteomics. 2011;10(8):M110.007187.
  94. Xu W, Hu H, Wang Z, Chen X, Yang F, Zhu Z, et al. Proteomic characteristics of spermatozoa in normozoospermic patients with infertility. J Proteomics. 2012;75(17):5426-36.
  95. Parte PP, Rao P, Redij S, Lobo V, D'Souza SJ, Gajbhiye R, et al. Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC-MS(E)) reveals altered proteomic signatures in asthenozoospermia. J Proteomics. 2012;75(18):5861-71.
  96. Redgrove KA, Nixon B, Baker MA, Hetherington L, Baker G, Liu DY, et al. The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS One. 2012;7(11):e50851.
  97. Shen S, Wang J, Liang J, He D. Comparative proteomic study between human normal motility sperm and idiopathic asthenozoospermia. World J Urol. 2013;31(6):1395-401.
  98. Behrouzi B, Kenigsberg S, Alladin N, Swanson S, Zicherman J, Hong SH, et al. Evaluation of potential protein biomarkers in patients with high sperm DNA damage. Syst Biol Reprod Med. 2013;59(3):153-63.
  99. Kichine E, Di Falco M, Hales BF, Robaire B, Chan P. Analysis of the sperm head protein profiles in fertile men: consistency across time in the levels of expression of heat shock proteins and peroxiredoxins. PLoS One. 2013;8(10):e77471.
  100. Intasqui P, Camargo M, Del Giudice PT, Spaine DM, Carvalho VM, Cardozo KH, et al. Unraveling the sperm proteome and post-genomic pathways associated with sperm nuclear DNA fragmentation. J Assist Reprod Genet. 2013;30(9):1187-202.
  101. Zhu Y, Wu Y, Jin K, Lu H, Liu F, Guo Y, et al. Differential proteomic profiling in human spermatozoa that did or did not result in pregnancy via IVF and AID. Proteomics Clin Appl. 2013;7(11-12):850-8.
  102. Azpiazu R, Amaral A, Castillo J, Estanyol JM, Guimerà M, Ballescà JL, et al. High-throughput sperm differential proteomics suggests that epigenetic alterations contribute to failed assisted reproduction. Hum Reprod. 2014;29(6):1225-37.
  103. Wang S, Wang W, Xu Y, Tang M, Fang J, Sun H, et al. Proteomic characteristics of human sperm cryopreservation. Proteomics. 2014;14(2-3):298-310.
  104. Pilatz A, Lochnit G, Karnati S, Paradowska-Dogan A, Lang T, Schultheiss D, et al. Acute epididymitis induces alterations in sperm protein composition. Fertil Steril. 2014;101(6):1609-17.e1-5.
  105. Frapsauce C, Pionneau C, Bouley J, Delarouziere V, Berthaut I, Ravel C, et al. Proteomic identification of target proteins in normal but nonfertilizing sperm. Fertil Steril. 2014;102(2):372-80.
  106. McReynolds S, Dzieciatkowska M, Stevens J, Hansen KC, Schoolcraft WB, Katz-Jaffe MG. Toward the identification of a subset of unexplained infertility: a sperm proteomic approach. Fertil Steril. 2014;102(3):692-9.
  107. Liu Y, Guo Y, Song N, Fan Y, Li K, Teng X, et al. Proteomic pattern changes associated with obesity-induced asthenozoospermia. Andrology. 2015;3(2):247-59.
  108. Amaral A, Castillo J, Estanyol JM, Ballescà JL, Ramalho-Santos J, Oliva R. Human sperm tail proteome suggests new endogenous metabolic pathways. Mol Cell Proteomics. 2013;12(2):330-42.
  109. Cui Z, Sharma R, Agarwal A. Proteomic analysis of mature and immature ejaculated spermatozoa from fertile men. Asian J Androl. 2016;18(5):735-46.
  110. Amaral A, Paiva C, Attardo Parrinello C, Estanyol JM, Ballescà JL, Ramalho-Santos J, et al. Identification of proteins involved in human sperm motility using high-throughput differential proteomics. J Proteome Res. 2014;13(12):5670-84.
Journal of Reproduction & Infertility
Volume 18, Issue 3
Summer 2017
Pages 267-279