Skip to main content
Top
Published in: BMC Urology 1/2019

Open Access 01-12-2019 | Fertility | Research article

Quantitative proteomic characterization of human sperm cryopreservation: using data-independent acquisition mass spectrometry

Authors: Longlong Fu, Qi An, Kaishu Zhang, Ying Liu, Yue Tong, Jianfeng Xu, Fang Zhou, Xiaowei Wang, Ying Guo, Wenhong Lu, Xiaowei Liang, Yiqun Gu

Published in: BMC Urology | Issue 1/2019

Login to get access

Abstract

Background

Human sperm cryopreservation is a simple and effective approach for male fertility preservation.

Methods

To identify potential proteomic changes in this process, data-independent acquisition (DIA), a technology with high quantitative accuracy and highly reproducible proteomics, was used to quantitatively characterize the proteomics of human sperm cryopreservation.

Results

A total of 174 significantly differential proteins were identified between fresh and cryoperservated sperm: 98 proteins decreased and 76 proteins increased in the cryopreservation group. Bioinformatic analysis revealed that metabolic pathways play an important role in cryopreservation, including: propanoate metabolism, glyoxylate and dicarboxylate metabolism, glycolysis/gluconeogenesis, and pyruvate metabolism. Four different proteins involved in glycolysis were identified by Western blotting: GPI, LDHB, ADH5, and PGAM1.

Conclusions

Our work will provide valuable information for future investigations and pathological studies involving sperm cryopreservation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Yogev L, Kleiman SE, Shabtai E, Botchan A, Paz G, Hauser R, Lehavi O, Yavetz H, Gamzu R. Long-term cryostorage of sperm in a human sperm bank does not damage progressive motility concentration. Hum Reprod. 2010;25(5):1097–103.CrossRef Yogev L, Kleiman SE, Shabtai E, Botchan A, Paz G, Hauser R, Lehavi O, Yavetz H, Gamzu R. Long-term cryostorage of sperm in a human sperm bank does not damage progressive motility concentration. Hum Reprod. 2010;25(5):1097–103.CrossRef
2.
go back to reference Tournaye H, Dohle GR, Barratt CL. Fertility preservation in men with cancer. Lancet. 2014;384(9950):1295–301.CrossRef Tournaye H, Dohle GR, Barratt CL. Fertility preservation in men with cancer. Lancet. 2014;384(9950):1295–301.CrossRef
3.
go back to reference Oktay K, Harvey BE, Partridge AH, Quinn GP, Reinecke J, Taylor HS, Wallace WH, Wang ET, Loren AW. Fertility Preservation in Patients With Cancer: ASCO Clinical Practice Guideline Update. J Clin Oncol. 2018;36(19):1994-2001.CrossRef Oktay K, Harvey BE, Partridge AH, Quinn GP, Reinecke J, Taylor HS, Wallace WH, Wang ET, Loren AW. Fertility Preservation in Patients With Cancer: ASCO Clinical Practice Guideline Update. J Clin Oncol. 2018;36(19):1994-2001.CrossRef
4.
go back to reference Fu L, Zhang K, An Q, Zhou F, Lu W, Liang X, Gu Y. Low utilization of fertility preservation among Chinese male cancer patients. Int J Clin Exp Med. 2018;11(9):9916–20. Fu L, Zhang K, An Q, Zhou F, Lu W, Liang X, Gu Y. Low utilization of fertility preservation among Chinese male cancer patients. Int J Clin Exp Med. 2018;11(9):9916–20.
5.
go back to reference Raad G, Lteif L, Lahoud R, Azoury J, Azoury J, Tanios J, Hazzouri M, Azoury J. Cryopreservation media differentially affect sperm motility, morphology and DNA integrity. Andrology. 2018;6(6):836-45.CrossRef Raad G, Lteif L, Lahoud R, Azoury J, Azoury J, Tanios J, Hazzouri M, Azoury J. Cryopreservation media differentially affect sperm motility, morphology and DNA integrity. Andrology. 2018;6(6):836-45.CrossRef
6.
go back to reference Gomez-Torres MJ, Medrano L, Romero A, Fernandez-Colom PJ, Aizpurua J. Effectiveness of human spermatozoa biomarkers as indicators of structural damage during cryopreservation. Cryobiology. 2017;78:90–4.CrossRef Gomez-Torres MJ, Medrano L, Romero A, Fernandez-Colom PJ, Aizpurua J. Effectiveness of human spermatozoa biomarkers as indicators of structural damage during cryopreservation. Cryobiology. 2017;78:90–4.CrossRef
7.
go back to reference Ribas-Maynou J, Fernandez-Encinas A, Garcia-Peiro A, Prada E, Abad C, Amengual MJ, Navarro J, Benet J. Human semen cryopreservation: a sperm DNA fragmentation study with alkaline and neutral comet assay. Andrology. 2014;2(1):83–7.CrossRef Ribas-Maynou J, Fernandez-Encinas A, Garcia-Peiro A, Prada E, Abad C, Amengual MJ, Navarro J, Benet J. Human semen cryopreservation: a sperm DNA fragmentation study with alkaline and neutral comet assay. Andrology. 2014;2(1):83–7.CrossRef
8.
go back to reference Kathrins M, Abhyankar N, Shoshany O, Liebermann J, Uhler M, Prins G, Niederberger C. Post-thaw recovery of rare or very low concentrations of cryopreserved human sperm. Fertil Steril. 2017;107(6):1300–4.CrossRef Kathrins M, Abhyankar N, Shoshany O, Liebermann J, Uhler M, Prins G, Niederberger C. Post-thaw recovery of rare or very low concentrations of cryopreserved human sperm. Fertil Steril. 2017;107(6):1300–4.CrossRef
9.
go back to reference De Rose MB, Piccolomini MM, Belo ASS, Borges E, Jr., Filho FF: Proteomics in Human Reproduction. Protein and peptide letters 2018. De Rose MB, Piccolomini MM, Belo ASS, Borges E, Jr., Filho FF: Proteomics in Human Reproduction. Protein and peptide letters 2018.
10.
go back to reference Cao X, Cui Y, Zhang X, Lou J, Zhou J, Bei H, Wei R. Proteomic profile of human spermatozoa in healthy and asthenozoospermic individuals. Reprod Biol Endocrinol. 2018;16(1):16.CrossRef Cao X, Cui Y, Zhang X, Lou J, Zhou J, Bei H, Wei R. Proteomic profile of human spermatozoa in healthy and asthenozoospermic individuals. Reprod Biol Endocrinol. 2018;16(1):16.CrossRef
11.
go back to reference Tsou CC, Avtonomov D, Larsen B, Tucholska M, Choi H, Gingras AC, Nesvizhskii AI. DIA-Umpire: comprehensive computational framework for data-independent acquisition proteomics. Nat Methods. 2015;12(3):258–64 257 p following 264.CrossRef Tsou CC, Avtonomov D, Larsen B, Tucholska M, Choi H, Gingras AC, Nesvizhskii AI. DIA-Umpire: comprehensive computational framework for data-independent acquisition proteomics. Nat Methods. 2015;12(3):258–64 257 p following 264.CrossRef
12.
go back to reference Yang X, Guo Y, Cao XF, Jia YF, Wang XW, Xu JF, Zhou F, Li H, Liang XW, Lu WH, et al. Effect of cryopreservation on DNA methylation status of imprited genes in human sperm. J Reprod Medcine. 2015;24(5):402–8. Yang X, Guo Y, Cao XF, Jia YF, Wang XW, Xu JF, Zhou F, Li H, Liang XW, Lu WH, et al. Effect of cryopreservation on DNA methylation status of imprited genes in human sperm. J Reprod Medcine. 2015;24(5):402–8.
13.
go back to reference Wang S, Wang W, Xu Y, Tang M, Fang J, Sun H, Sun Y, Gu M, Liu Z, Zhang Z, et al. Proteomic characteristics of human sperm cryopreservation. Proteomics. 2014;14(2–3):298–310.CrossRef Wang S, Wang W, Xu Y, Tang M, Fang J, Sun H, Sun Y, Gu M, Liu Z, Zhang Z, et al. Proteomic characteristics of human sperm cryopreservation. Proteomics. 2014;14(2–3):298–310.CrossRef
14.
go back to reference Hezavehei M, Sharafi M, Kouchesfahani HM, Henkel R, Agarwal A, Esmaeili V, Shahverdi A. Sperm cryopreservation: a review on current molecular cryobiology and advanced approaches. Reprod BioMed Online. 2018;37(3):327–39.CrossRef Hezavehei M, Sharafi M, Kouchesfahani HM, Henkel R, Agarwal A, Esmaeili V, Shahverdi A. Sperm cryopreservation: a review on current molecular cryobiology and advanced approaches. Reprod BioMed Online. 2018;37(3):327–39.CrossRef
15.
go back to reference Wang G, Wu Y, Zhou T, Guo Y, Zheng B, Wang J, Bi Y, Liu F, Zhou Z, Guo X, et al. Mapping of the N-linked glycoproteome of human spermatozoa. J Proteome Res. 2013;12(12):5750–9.CrossRef Wang G, Wu Y, Zhou T, Guo Y, Zheng B, Wang J, Bi Y, Liu F, Zhou Z, Guo X, et al. Mapping of the N-linked glycoproteome of human spermatozoa. J Proteome Res. 2013;12(12):5750–9.CrossRef
16.
go back to reference Li F, Zhao D, Yang S, Wang J, Liu Q, Jin X, Wang W. ITRAQ-based proteomics analysis of Triptolide on human A549 lung adenocarcinoma cells. Cell Physiol Biochem. 2018;45(3):917–34.CrossRef Li F, Zhao D, Yang S, Wang J, Liu Q, Jin X, Wang W. ITRAQ-based proteomics analysis of Triptolide on human A549 lung adenocarcinoma cells. Cell Physiol Biochem. 2018;45(3):917–34.CrossRef
17.
go back to reference Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–d361.CrossRef Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–d361.CrossRef
18.
go back to reference Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447–52.CrossRef Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447–52.CrossRef
19.
go back to reference Liu Y, Wang J, Qin Y, Huang C, Archacki S, Ma J, Li D, Liu M. Identification of three mutations in the MVK gene in six patients associated with disseminated superficial actinic porokeratosis. Clinica Chimica Acta; Int J Clin Chem. 2016;454:124–9.CrossRef Liu Y, Wang J, Qin Y, Huang C, Archacki S, Ma J, Li D, Liu M. Identification of three mutations in the MVK gene in six patients associated with disseminated superficial actinic porokeratosis. Clinica Chimica Acta; Int J Clin Chem. 2016;454:124–9.CrossRef
20.
go back to reference Agarwal A, Mulgund A, Hamada A, Chyatte MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 2015;13:37.CrossRef Agarwal A, Mulgund A, Hamada A, Chyatte MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 2015;13:37.CrossRef
21.
go back to reference Nahata L, Caltabellotta NM, Yeager ND, Lehmann V, Whiteside SL, O'Brien SH, Quinn GP, Gerhardt CA: Fertility perspectives and priorities among male adolescents and young adults in cancer survivorship. Pediatric blood & cancer 2018. Nahata L, Caltabellotta NM, Yeager ND, Lehmann V, Whiteside SL, O'Brien SH, Quinn GP, Gerhardt CA: Fertility perspectives and priorities among male adolescents and young adults in cancer survivorship. Pediatric blood & cancer 2018.
22.
go back to reference Isaac AV, Kumari S, Nair R, Urs DR, Salian SR, Kalthur G, Adiga SK, Manikkath J, Mutalik S, Sachdev D, et al. Supplementing zinc oxide nanoparticles to cryopreservation medium minimizes the freeze-thaw-induced damage to spermatozoa. Biochem Biophys Res Commun. 2017;494(3–4):656–62.CrossRef Isaac AV, Kumari S, Nair R, Urs DR, Salian SR, Kalthur G, Adiga SK, Manikkath J, Mutalik S, Sachdev D, et al. Supplementing zinc oxide nanoparticles to cryopreservation medium minimizes the freeze-thaw-induced damage to spermatozoa. Biochem Biophys Res Commun. 2017;494(3–4):656–62.CrossRef
23.
go back to reference Cao WL, Wang YX, Xiang ZQ, Li Z. Cryopreservation-induced decrease in heat-shock protein 90 in human spermatozoa and its mechanism. Asian J Androl. 2003;5(1):43–6.PubMed Cao WL, Wang YX, Xiang ZQ, Li Z. Cryopreservation-induced decrease in heat-shock protein 90 in human spermatozoa and its mechanism. Asian J Androl. 2003;5(1):43–6.PubMed
24.
go back to reference Li CJ, Wang D, Zhou X. Sperm proteome and reproductive technologies in mammals. Anim Reprod Sci. 2016;173:1–7.CrossRef Li CJ, Wang D, Zhou X. Sperm proteome and reproductive technologies in mammals. Anim Reprod Sci. 2016;173:1–7.CrossRef
25.
go back to reference Kosteria I, Anagnostopoulos AK, Kanaka-Gantenbein C, Chrousos GP, Tsangaris GT. The Use of Proteomics in Assisted Reproduction. In Vivo (Athens, Greece). 2017;31(3):267–83. Kosteria I, Anagnostopoulos AK, Kanaka-Gantenbein C, Chrousos GP, Tsangaris GT. The Use of Proteomics in Assisted Reproduction. In Vivo (Athens, Greece). 2017;31(3):267–83.
26.
go back to reference Bogle OA, Kumar K, Attardo-Parrinello C, Lewis SE, Estanyol JM, Ballesca JL, Oliva R. Identification of protein changes in human spermatozoa throughout the cryopreservation process. Andrology. 2017;5(1):10–22.CrossRef Bogle OA, Kumar K, Attardo-Parrinello C, Lewis SE, Estanyol JM, Ballesca JL, Oliva R. Identification of protein changes in human spermatozoa throughout the cryopreservation process. Andrology. 2017;5(1):10–22.CrossRef
27.
go back to reference Muntel J, Xuan Y, Berger ST, Reiter L, Bachur R, Kentsis A, Steen H. Advancing urinary protein biomarker discovery by data-independent acquisition on a Quadrupole-Orbitrap mass spectrometer. J Proteome Res. 2015;14(11):4752–62.CrossRef Muntel J, Xuan Y, Berger ST, Reiter L, Bachur R, Kentsis A, Steen H. Advancing urinary protein biomarker discovery by data-independent acquisition on a Quadrupole-Orbitrap mass spectrometer. J Proteome Res. 2015;14(11):4752–62.CrossRef
28.
go back to reference Meyer JG, D'Souza AK, Sorensen DJ, Rardin MJ, Wolfe AJ, Gibson BW, Schilling B. Quantification of lysine acetylation and Succinylation stoichiometry in proteins using mass spectrometric data-independent acquisitions (SWATH). J Am Soc Mass Spectrom. 2016;27(11):1758–71.CrossRef Meyer JG, D'Souza AK, Sorensen DJ, Rardin MJ, Wolfe AJ, Gibson BW, Schilling B. Quantification of lysine acetylation and Succinylation stoichiometry in proteins using mass spectrometric data-independent acquisitions (SWATH). J Am Soc Mass Spectrom. 2016;27(11):1758–71.CrossRef
29.
go back to reference Chen L, Lu D, Sun K, Xu Y, Hu P, Li X, Xu F. Identification of biomarkers associated with diagnosis and prognosis of colorectal cancer patients based on integrated bioinformatics analysis. Gene. 2019. Chen L, Lu D, Sun K, Xu Y, Hu P, Li X, Xu F. Identification of biomarkers associated with diagnosis and prognosis of colorectal cancer patients based on integrated bioinformatics analysis. Gene. 2019.
30.
go back to reference Zhang Y, Tang X, Pang Y, Huang L, Wang D, Yuan C, Hu X, Qu L. The Potential Mechanism of Bufadienolide-Like Chemicals on Breast Cancer via Bioinformatics Analysis. Cancers (Basel). 2019;11(1):91.CrossRef Zhang Y, Tang X, Pang Y, Huang L, Wang D, Yuan C, Hu X, Qu L. The Potential Mechanism of Bufadienolide-Like Chemicals on Breast Cancer via Bioinformatics Analysis. Cancers (Basel). 2019;11(1):91.CrossRef
31.
go back to reference Singh K, Jaiswal D. One-carbon metabolism, spermatogenesis, and male infertility. Reprod Sci (Thousand Oaks, Calif). 2013;20(6):622–30.CrossRef Singh K, Jaiswal D. One-carbon metabolism, spermatogenesis, and male infertility. Reprod Sci (Thousand Oaks, Calif). 2013;20(6):622–30.CrossRef
32.
go back to reference du Plessis SS, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use? Asian J Androl. 2015;17(2):230–5.CrossRef du Plessis SS, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use? Asian J Androl. 2015;17(2):230–5.CrossRef
33.
go back to reference Gibb Z, Aitken RJ. The impact of sperm metabolism during in vitro storage: the stallion as a model. Biomed Res Int. 2016;2016:9380609.CrossRef Gibb Z, Aitken RJ. The impact of sperm metabolism during in vitro storage: the stallion as a model. Biomed Res Int. 2016;2016:9380609.CrossRef
34.
go back to reference Hereng TH, Elgstoen KB, Cederkvist FH, Eide L, Jahnsen T, Skalhegg BS, Rosendal KR. Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum Reprod. 2011;26(12):3249–63.CrossRef Hereng TH, Elgstoen KB, Cederkvist FH, Eide L, Jahnsen T, Skalhegg BS, Rosendal KR. Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum Reprod. 2011;26(12):3249–63.CrossRef
35.
go back to reference Stendardi A, Focarelli R, Piomboni P, Palumberi D, Serafini F, Ferramosca A, Zara V. Evaluation of mitochondrial respiratory efficiency during in vitro capacitation of human spermatozoa. Int J Androl. 2011;34(3):247–55.CrossRef Stendardi A, Focarelli R, Piomboni P, Palumberi D, Serafini F, Ferramosca A, Zara V. Evaluation of mitochondrial respiratory efficiency during in vitro capacitation of human spermatozoa. Int J Androl. 2011;34(3):247–55.CrossRef
36.
go back to reference O'Connell M, McClure N, Lewis SE. The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum Reprod. 2002;17(3):704–9.CrossRef O'Connell M, McClure N, Lewis SE. The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum Reprod. 2002;17(3):704–9.CrossRef
37.
go back to reference Jiang XP, Wang SQ, Wang W, Xu Y, Xu Z, Tang JY, Sun HY, Wang ZJ, Zhang W. Enolase1 (ENO1) and glucose-6-phosphate isomerase (GPI) are good markers to predict human sperm freezability. Cryobiology. 2015;71(1):141–5.CrossRef Jiang XP, Wang SQ, Wang W, Xu Y, Xu Z, Tang JY, Sun HY, Wang ZJ, Zhang W. Enolase1 (ENO1) and glucose-6-phosphate isomerase (GPI) are good markers to predict human sperm freezability. Cryobiology. 2015;71(1):141–5.CrossRef
38.
go back to reference Li P, Guo W, Yue H, Li C, Du H, Qiao X, Liu Z, Zhou Q, Wei Q. Variability in the protein profiles in spermatozoa of two sturgeon species. PLoS One. 2017;12(10):e0186003.CrossRef Li P, Guo W, Yue H, Li C, Du H, Qiao X, Liu Z, Zhou Q, Wei Q. Variability in the protein profiles in spermatozoa of two sturgeon species. PLoS One. 2017;12(10):e0186003.CrossRef
39.
go back to reference Zhang S, Zhao Y, Lei B, Li C, Mao X. PGAM1 is Involved in Spermatogenic Dysfunction and Affects Cell Proliferation, Apoptosis, and Migration. Reprod Sci (Thousand Oaks, Calif). 2015;22(10):1236–42.CrossRef Zhang S, Zhao Y, Lei B, Li C, Mao X. PGAM1 is Involved in Spermatogenic Dysfunction and Affects Cell Proliferation, Apoptosis, and Migration. Reprod Sci (Thousand Oaks, Calif). 2015;22(10):1236–42.CrossRef
40.
go back to reference Aly HA, El-Beshbishy HA, Banjar ZM. Mitochondrial dysfunction induced impairment of spermatogenesis in LPS-treated rats: modulatory role of lycopene. Eur J Pharmacol. 2012;677(1–3):31–8.CrossRef Aly HA, El-Beshbishy HA, Banjar ZM. Mitochondrial dysfunction induced impairment of spermatogenesis in LPS-treated rats: modulatory role of lycopene. Eur J Pharmacol. 2012;677(1–3):31–8.CrossRef
Metadata
Title
Quantitative proteomic characterization of human sperm cryopreservation: using data-independent acquisition mass spectrometry
Authors
Longlong Fu
Qi An
Kaishu Zhang
Ying Liu
Yue Tong
Jianfeng Xu
Fang Zhou
Xiaowei Wang
Ying Guo
Wenhong Lu
Xiaowei Liang
Yiqun Gu
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Fertility
Published in
BMC Urology / Issue 1/2019
Electronic ISSN: 1471-2490
DOI
https://doi.org/10.1186/s12894-019-0565-2

Other articles of this Issue 1/2019

BMC Urology 1/2019 Go to the issue