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Quantitative proteomics of sperm tail in asthenozoospermic patients: exploring the molecular pathways affecting sperm motility

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Abstract

Asthenozoospermia, characterized by low sperm motility, is one of the most common causes of male infertility. While many intrinsic and extrinsic factors are involved in the etiology of asthenozoospermia, the molecular basis of this condition remains unclear. Since sperm motility results from a complex flagellar structure, an in-depth proteomic analysis of the sperm tail can uncover mechanisms underlying asthenozoospermia. This study quantified the proteomic profile of 40 asthenozoospermic sperm tails and 40 controls using TMT-LC–MS/MS. Overall, 2140 proteins were identified and quantified where 156 proteins have not been described earlier in sperm tail. There were 409 differentially expressed proteins (250 upregulated and 159 downregulated) in asthenozoospermia which by far is the highest number reported earlier. Further, bioinformatics analysis revealed several biological processes, including mitochondrial-related energy production, oxidative phosphorylation (OXPHOS), citric acid cycle (CAC), cytoskeleton, stress response, and protein metabolism altered in asthenozoospermic sperm tail samples. Collectively, our findings reveal the importance of mitochondrial energy production and induced stress response as potential mechanisms involved in the loss of sperm motility in asthenozoospermia.

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References

  • Agarwal A, Bertolla RP, Samanta L (2016) Sperm proteomics: potential impact on male infertility treatment. Expert Rev Proteomics 13:285–296

    Article  CAS  PubMed  Google Scholar 

  • Amaral A, Castillo J, Estanyol J, Lagarda JL, Ramalho-Santos J, Oliva R (2012) Human sperm tail proteome suggests new endogenous metabolic pathways. Mol Cell Proteomics 12

  • Amaral A, Castillo J, Ramalho-Santos J, Oliva R (2014a) The combined human sperm proteome: cellular pathways and implications for basic and clinical science. Hum Reprod Update 20:40–62

    Article  CAS  PubMed  Google Scholar 

  • Amaral A, Paiva C, Attardo Parrinello C, Estanyol JM, Ballescà JL, Ramalho-Santos J, Oliva R (2014b) Identification of proteins involved in human sperm motility using high-throughput differential proteomics. J Proteome Res 13:5670–5684

    Article  CAS  PubMed  Google Scholar 

  • Amaral A, Paiva C, Baptista M, Sousa AP, Ramalho-Santos J (2011) Exogenous glucose improves long-standing human sperm motility, viability, and mitochondrial function. Fertil Steril 96:848–850

    Article  CAS  PubMed  Google Scholar 

  • Amaral A, Ramalho-Santos J (2010) Assessment of mitochondrial potential: implications for the correct monitoring of human sperm function. Int J Androl 33:e180–e186

    Article  CAS  PubMed  Google Scholar 

  • Ariumi Y (2014) Multiple functions of DDX3 RNA helicase in gene regulation, tumorigenesis, and viral infection. Front Genet 5:423

    Article  PubMed  PubMed Central  Google Scholar 

  • Asghari A, Marashi S-A, Ansari-Pour N (2017) A sperm-specific proteome-scale metabolic network model identifies non-glycolytic genes for energy deficiency in asthenozoospermia. Syst Biol Reprod Med 63:100–112

    Article  CAS  PubMed  Google Scholar 

  • Baker MA, Naumovski N, Hetherington L, Weinberg A, Velkov T, Aitken RJ (2013) Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 13:61–74

    Article  CAS  PubMed  Google Scholar 

  • Bansal SK, Gupta N, Sankhwar SN, Rajender S (2015) Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PloS One 10

  • Brewis IA, Brennan P (2010) Proteomics technologies for the global identification and quantification of proteins. Advances in protein chemistry and structural biology, vol 80. Elsevier, pp 1–44

  • Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304:596–600

    Article  CAS  PubMed  Google Scholar 

  • Byagowi S, Naserpour Farivar T, Najafipour R, Sahmani M, Darabi M, Fayezi S, Mirshahvaladi S, Darabi M (2015) Effect of PPARδ agonist on stearoyl-CoA desaturase 1 in human pancreatic cancer cells: role of MEK/ERK1/2 pathway. Can J Diabetes 39:123–127

    Article  PubMed  Google Scholar 

  • Cao X, Cui Y, Zhang X, Lou J, Zhou J, Bei H, Wei R (2018) Proteomic profile of human spermatozoa in healthy and asthenozoospermic individuals. Reprod Biol Endocrinol 16:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Chan C-C, Shui H-A, Wu C-H, Wang C-Y, Sun G-H, Chen H-M, Wu G-J (2009) Motility and protein phosphorylation in healthy and asthenozoospermic sperm. J Proteome Res 8:5382–5386

    Article  CAS  PubMed  Google Scholar 

  • Chandramouli K, Qian P-Y (2009) Proteomics: challenges, techniques and possibilities to overcome biological sample complexity. Hum Genomics Proteomics HGP 2009

  • Conway JR, Lex A, Gehlenborg N (2017) UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics 33:2938–2940

    Article  CAS  PubMed Central  Google Scholar 

  • Curi S, Ariagno J, Chenlo P, Mendeluk G, Pugliese M, Sardi Segovia L, Repetto H, Blanco A (2003) asthenozoospermia: analysis of a large population. Arch Androl 49:343–349

    Article  CAS  PubMed  Google Scholar 

  • Deng L, Pushpitha K, Joseph C, Gupta V, Rajput R, Chitranshi N, Dheer Y, Amirkhani A, Kamath K, Pascovici D, Wu JX, Salekdeh GH, Haynes PA, Graham SL, Gupta VK, Mirzaei M (2019) Amyloid β induces early changes in the ribosomal machinery, cytoskeletal organization and oxidative phosphorylation in retinal photoreceptor cells. Front Mol Neurosci 12:24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ditton H, Zimmer J, Kamp C, Rajpert-De Meyts E, Vogt P (2004) The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control. Hum Mol Genet 13:2333–2341

    Article  CAS  PubMed  Google Scholar 

  • Doncheva NT, Morris JH, Gorodkin J, Jensen LJ (2018) Cytoscape StringApp: network analysis and visualization of proteomics data. J Proteome Res 18:623–632

    Article  PubMed  PubMed Central  Google Scholar 

  • du Plessis SS, Kashou AH, Benjamin DJ, Yadav SP, Agarwal A (2011) Proteomics: a subcellular look at spermatozoa. Reprod Biol Endocrinol 9:36–36

    Article  PubMed  PubMed Central  Google Scholar 

  • Du Y, Li M, Chen J, Duan Y, Wang X, Qiu Y, Cai Z, Gui Y, Jiang H (2016) Promoter targeted bisulfite sequencing reveals DNA methylation profiles associated with low sperm motility in asthenozoospermia. Hum Reprod 31:24–33

    Article  CAS  PubMed  Google Scholar 

  • Ergur AR, Dokras A, Giraldo JL, Habana A, Kovanci E, Huszar G (2002) Sperm maturity and treatment choice of in vitro fertilization (IVF) or intracytoplasmic sperm injection: diminished sperm HspA2 chaperone levels predict IVF failure. Fertil Steril 77:910–918

    Article  PubMed  Google Scholar 

  • Folgerø T, Bertheussen K, Lindal S, Torbergsen T, Øian P (1993) Andrology: mitochondrial disease and reduced sperm motility. Hum Reprod 8:1863–1868

    Article  PubMed  Google Scholar 

  • Garrido C, Solary E (2003) A role of HSPs in apoptosis through “protein triage”? Nature Publishing Group

  • GeneCards (2022) Gene Cards – the human gene database

  • Gilany K, Lakpour N, Vafakhah M, Sadeghi MR (2011) The profile of human sperm proteome; a mini-review. J Reprod Infertil 12:193–199

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gòdia M, Swanson G, Krawetz SA (2018) A history of why fathers’ RNA matters. Biol Reprod 99

  • Gu Z, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32:2847–2849

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Jiang W, Yu W, Niu X, Liu F, Zhou T, Zhang H, Li Y, Zhu H, Zhou Z (2019) Proteomics analysis of asthenozoospermia and identification of glucose-6-phosphate isomerase as an important enzyme for sperm motility. J Proteomics 208:103478

    Article  CAS  PubMed  Google Scholar 

  • Gur Y, Breitbart H (2006) Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20:411–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gur Y, Breitbart H (2008) Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Mol Cell Endocrinol 282:45–55

    Article  CAS  PubMed  Google Scholar 

  • Hashemitabar M, Sabbagh S, Orazizadeh M, Ghadiri A, Bahmanzadeh M (2015) A proteomic analysis on human sperm tail: comparison between normozoospermia and asthenozoospermia. J Assist Reprod Genet 32:853–863

    Article  PubMed  PubMed Central  Google Scholar 

  • Inaba K, Mizuno K (2016) Sperm dysfunction and ciliopathy. Reprod Med Biol 15:77–94

    Article  CAS  PubMed  Google Scholar 

  • Jodar M, Selvaraju S, Sendler E, Diamond M, Krawetz S, Network RM (2013) The presence, role and clinical use of spermatozoal RNAs. Hum Reprod Update 19

  • Khelifa MB, Coutton C, Zouari R, Karaouzène T, Rendu J, Bidart M, Yassine S, Pierre V, Delaroche J, Hennebicq S (2014) Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella. Am J Hum Genet 94:95–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuleshov MV, Jones MR, Rouillard AD, Fernandez NF, Duan Q, Wang Z, Koplev S, Jenkins SL, Jagodnik KM, Lachmann A, McDermott MG, Monteiro CD, Gundersen GW, Ma’ayan A (2016) Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res 44:W90–W97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai M-C, Lee Y-HW, Tarn W-Y (2008) The DEAD-Box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well asTip-associated protein and participates in translational control. Mol Biol Cell 19:3847–3858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YH, Tan HT, Chung MCM (2010) Subcellular fractionation methods and strategies for proteomics. Proteomics 10:3935–3956

    Article  CAS  PubMed  Google Scholar 

  • Lessley BA, Garner DL (1983) Isolation of motile spermatozoa by density gradient centrifugation in Percoll®. Gamete Res 7:49–61

    Article  Google Scholar 

  • Li HJ, Yu N, Zhang XY, Jin W, Li HZ (2010) Spermatozoal protein profiles in male infertility with asthenozoospermia. Chin Med J (engl) 123:2879–2882

    CAS  PubMed  Google Scholar 

  • Liu X, Teng Z, Wang Z, Zhu P, Song Z, Liu F (2022) Expressions of HSPA1L and HSPA9 are associated with poor sperm quality of low-motility spermatozoa in fertile men. Andrologia 54:e14321

    Article  CAS  PubMed  Google Scholar 

  • Luconi M, Baldi E (2003) How do sperm swim? Molecular mechanisms underlying sperm motility. Cell Mol Biol (Noisy-le-Grand, France) 49:357–369

    CAS  Google Scholar 

  • Luo W, Pant G, Bhavnasi YK, Blanchard SG Jr, Brouwer C (2017) Pathview Web: user friendly pathway visualization and data integration. Nucleic Acids Res 45:W501–W508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macleod G, Varmuza S (2013) The application of proteomic approaches to the study of mammalian spermatogenesis and sperm function. Febs J 280:5635–5651

    Article  CAS  PubMed  Google Scholar 

  • Manfrevola F, Ferraro B, Sellitto C, Rocco D, Fasano S, Pierantoni R, Chianese R (2021) CRISP2, CATSPER1 and PATE1 expression in human asthenozoospermic semen. Cells 10:1956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballesca JL, Oliva R (2008) Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 23:783–791

    Article  PubMed  Google Scholar 

  • Martínez-Heredia J, Estanyol JM, Ballescà JL, Oliva R (2006) Proteomic identification of human sperm proteins. Proteomics 6:4356–4369

    Article  PubMed  Google Scholar 

  • Mast FD, Ratushny AV, Aitchison JD (2014) Systems cell biology. J Cell Biol 206:695–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumura T, Endo T, Isotani A, Ogawa M, Ikawa M (2019) An azoospermic factor gene, Ddx3y and its paralog, Ddx3x are dispensable in germ cells for male fertility. J Reprod Dev 2018–2145

  • Mirzaei M, Abyadeh M, Turner AJ et al (2022) Fingolimod effects on the brain are mediated through biochemical modulation of bioenergetics, autophagy, and neuroinflammatory networks. Proteomics 22(19-20):e2100247. https://doi.org/10.1002/pmic.202100247

  • Mirzaei M, Gupta VB, Chick JM, Greco TM, Wu Y, Chitranshi N, Vander Wall R, Hone E, Deng L, Dheer Y (2017) Age-related neurodegenerative disease associated pathways identified in retinal and vitreous proteome from human glaucoma eyes. Sci Rep 7:1–16

    Article  Google Scholar 

  • Mobberley M (2010) Electron microscopy in the investigation of asthenozoospermia. Br J Biomed Sci 67:92–100

    Article  CAS  PubMed  Google Scholar 

  • Müller-McNicoll M, Rossbach O, Hui J, Medenbach J (2019) Auto-regulatory feedback by RNA-binding proteins. J Mol Cell Biol 11:930–939

    Article  PubMed  PubMed Central  Google Scholar 

  • Organization WH (2010a) Department of reproductive health and research. WHO Laboratory Manual for the Examination and Processing of Human Semen 5:21–22

    Google Scholar 

  • Boitrelle F, Shah R, Saleh R et al (2021) The sixth edition of the WHO manual for human semen analysis: A critical review and SWOT analysis. Life (Basel) 11(12):1368. Published 2021 Dec 9. https://doi.org/10.3390/life11121368

  • Ortega C, Verheyen G, Raick D, Camus M, Devroey P, Tournaye H (2011) Absolute asthenozoospermia and ICSI: what are the options? Hum Reprod Update 17:684–692

    Article  CAS  PubMed  Google Scholar 

  • Padmanabhan PK, Zghidi-Abouzid O, Samant M, Dumas C, Aguiar BG, Estaquier J, Papadopoulou B (2016) DDX3 DEAD-box RNA helicase plays a central role in mitochondrial protein quality control in Leishmania. Cell Death Dis 7:e2406–e2406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paulo JA, Gaun A, Kadiyala V, Ghoulidi A, Banks PA, Conwell DL, Steen H (2013) Subcellular fractionation enhances proteome coverage of pancreatic duct cells. Biochim Biophys Acta 1834:791–797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahimizadeh P, Topraggaleh TR, Nasr-Esfahani MH, Ziarati N, Mirshahvaladi S, Esmaeili V, Seifi S, Eftekhari-Yazdi P, Shahverdi A (2020) The alteration of PLCζ protein expression in unexplained infertile and asthenoteratozoospermic patients: a potential effect on sperm fertilization ability. Mol Reprod Dev 87:115–123

    Article  CAS  PubMed  Google Scholar 

  • Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A (2009) Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15:553–572

    Article  CAS  PubMed  Google Scholar 

  • Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J (2019) g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res 47:W191–W198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47–e47

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM (2007) Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. Faseb J 21:1013–1025

    Article  CAS  PubMed  Google Scholar 

  • Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM (2009) Tektin 3 is required for progressive sperm motility in mice. Mol Reprod Dev Inc Gamete Res 76:453–459

    Article  CAS  Google Scholar 

  • Salvolini E, Buldreghini E, Lucarini G, Vignini A, Lenzi A, Di Primio R, Balercia G (2013) Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility. Fertil Steril 99:697–704

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sendler E, Johnson GD, Mao S, Goodrich RJ, Diamond MP, Hauser R, Krawetz SA (2013) Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res 41

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen S, Wang J, Liang J, He D (2013) Comparative proteomic study between human normal motility sperm and idiopathic asthenozoospermia. World J Urol 31:1395–1401

    Article  CAS  PubMed  Google Scholar 

  • Shih J-W, Wang W-T, Tsai T-Y, Kuo C-Y, Li H-K, Wu Lee Y-H (2011) Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. Biochem J 441:119–129

    Article  Google Scholar 

  • Siva AB, Kameshwari DB, Singh V, Pavani K, Sundaram CS, Rangaraj N, Deenadayal M, Shivaji S (2010) Proteomics-based study on asthenozoospermia: differential expression of proteasome alpha complex. Mol Hum Reprod 16:452–462

    Article  CAS  PubMed  Google Scholar 

  • Storey BT (2004) Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52:427–437

    Article  Google Scholar 

  • Tanaka H, Iguchi N, Toyama Y, Kitamura K, Takahashi T, Kaseda K, Maekawa M, Nishimune Y (2004) Mice deficient in the axonemal protein Tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol Cell Biol 24:7958–7964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor CF, Paton NW, Lilley KS, Binz P-A, Julian RK, Jones AR, Zhu W, Apweiler R, Aebersold R, Deutsch EW (2007) The minimum information about a proteomics experiment (MIAPE). Nat Biotechnol 25:887–893

    Article  CAS  PubMed  Google Scholar 

  • Turner RM (2003) Tales from the tail: what do we really know about sperm motility? J Androl 24:790–803

    Article  PubMed  Google Scholar 

  • Turner RM (2005) Moving to the beat: a review of mammalian sperm motility regulation. Reprod Fertil Dev 18:25–38

    Article  Google Scholar 

  • Wasinger VC, Zeng M, Yau Y (2013) Current status and advances in quantitative proteomic mass spectrometry. Int J Proteomics 2013

  • Wilhelm M, Schlegl J, Hahne H, Gholami AM, Lieberenz M, Savitski MM, Ziegler E, Butzmann L, Gessulat S, Marx H (2014) Mass-spectrometry-based draft of the human proteome. Nature 509:582–587

    Article  CAS  PubMed  Google Scholar 

  • Wright P, Noirel J, Ow S-Y, Fazeli A (2012) A review of current proteomics technologies with a survey on their widespread use in reproductive biology investigations. Theriogenology 77(738–765):e752

    Google Scholar 

  • Yates JR 3rd, Gilchrist A, Howell KE, Bergeron JJ (2005) Proteomics of organelles and large cellular structures. Nat Rev Mol Cell Biol 6:702–714

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Huo R, Wang F-Q, Lin M, Zhou Z-M, Sha J-H (2007) Identification of several proteins involved in regulation of sperm motility by proteomic analysis. Fertil Steril 87:436–438

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Yang Q, Xu J, Zhao W, Zhang Z, Xu D, Zhang Y, Zhao E, Zhao G (2019) Somatic mutation of DNAH genes implicated higher chemotherapy response rate in gastric adenocarcinoma patients. J Transl Med 17:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuccarello D, Ferlin A, Garolla A, Pati MA, Moretti A, Cazzadore C, Francavilla S, Foresta C (2008) A possible association of a human tektin-t gene mutation (A229V) with isolated non-syndromic asthenozoospermia: case report. Hum Reprod 23:996–1001

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We express our heartfelt appreciation to Morteza Abyadeh for his great help in writing this manuscript. We also thank Mehdi Alikhani for helping with preliminary data analysis and providing valuable contributions.

Funding

This work was supported by a research grant (91000398) from the Royan Institute.

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TRT and ASH conceived the idea and designed the study. SM performed mass spectrometry and bioinformatic analysis. TRT, SM, and PR carried out the experiments. The first draft was written by TRT and completed by MNB. All authors read and edited the final version of the manuscript.

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Correspondence to Tohid Rezaei Topraggaleh or Abdolhossein Shahverdi.

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This case–control study was approved by the Institutional Ethics Committee of Royan Institute, Tehran, Iran (IR.ACECR.ROYAN.REC.1391.398).

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The written informed consents were signed before semen collection by patients referring to Royan Institute for assisted reproduction treatments. All cases were informed about using their clinical and biological data for this study.

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Mirshahvaladi, S., Topraggaleh, T.R., Bucak, M.N. et al. Quantitative proteomics of sperm tail in asthenozoospermic patients: exploring the molecular pathways affecting sperm motility. Cell Tissue Res 392, 793–810 (2023). https://doi.org/10.1007/s00441-023-03744-y

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