Insight into the complexity of male infertility: a multi-omics review

References

• Aderem A. 2005. Systems biology: its practice and challenges. Cell. 121(4):511–513. doi: 10.1016/j.cell.2005.04.020.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Mulgund A, Hamada A, Chyatte MR. 2015. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 13(1):37. doi: 10.1186/s12958-015-0032-1.
   PubMed Web of Science ®Google Scholar
• Bakey Z, Cabrera OA, Hoefele J, Antony D, Wu K, Stuck MW, Micha D, Eguether T, Smith AO, van der Wel NN, et al. 2023. IFT74 variants cause skeletal ciliopathy and motile cilia defects in mice and humans. PLoS Genet. 19(6):e1010796. doi: 10.1371/journal.pgen.1010796.
   PubMed Web of Science ®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(5):e0127007. doi: 10.1371/journal.pone.0127007.
   PubMed Web of Science ®Google Scholar
• Barišić A, Buretić Tomljanović A, Starčević Čizmarević N, Ostojić S, Romac P, Vraneković J. 2021. A rare Y-autosome translocation found in a patient with nonobstructive azoospermia: case report. Syst Biol Reprod Med. 67(4):307–313. doi: 10.1080/19396368.2021.1898701.
   PubMed Web of Science ®Google Scholar
• Berkay EG, Karaman B, Başaran S. 2023. A rare ring chromosome 21 abnormality is associated with azoospermia in two different phenotypically normal cases. Syst Biol Reprod Med. 69(5):387–393. doi: 10.1080/19396368.2023.2225682.
   PubMed Web of Science ®Google Scholar
• Bioinformatics. 2023. Calculate and draw custom Venn diagrams. Bioinformatics & evolutionary genomics; [accessed 12 Jan]. https://bioinformatics.psb.ugent.be/webtools/Venn/.
   Google Scholar
• Blaurock J, Baumann S, Grunewald S, Schiller J, Engel KM. 2022. Metabolomics of human semen: a review of different analytical methods to unravel biomarkers for male fertility disorders. Int J Mol Sci. 23(16):9031. doi: 10.3390/ijms23169031.
   PubMed Web of Science ®Google Scholar
• Coutton C, Vargas AS, Amiri-Yekta A, Kherraf ZE, Ben Mustapha SF, Le Tanno P, Wambergue-Legrand C, Karaouzène T, Martinez G, Crouzy S, et al. 2018. Mutations in CFAP43 and CFAP44 cause male infertility and flagellum defects in Trypanosoma and human. Nat Commun. 9(1):686. doi: 10.1038/s41467-017-02792-7.
   PubMedGoogle Scholar
• Dai X, Shen L. 2022. Advances and trends in omics technology development. Front Med. 9:911861. doi: 10.3389/fmed.2022.911861.
   Web of Science ®Google Scholar
• Danshina PV, Geyer CB, Dai Q, Goulding EH, Willis WD, Kitto GB, McCarrey JR, Eddy EM, O'Brien DA. 2010. Phosphoglycerate kinase 2 (PGK2) is essential for sperm function and male fertility in mice. Biol Reprod. 82(1):136–145. doi: 10.1095/biolreprod.109.079699.
   PubMed Web of Science ®Google Scholar
• Di Palma T, Filippone MG, Pierantoni GM, Fusco A, Soddu S, Zannini M. 2013. Pax8 has a critical role in epithelial cell survival and proliferation. Cell Death Dis. 4(7):e729. doi: 10.1038/cddis.2013.262.
   PubMedGoogle Scholar
• Djureinovic D, Fagerberg L, Hallström B, Danielsson A, Lindskog C, Uhlén M, Pontén F. 2014. The human testis-specific proteome defined by transcriptomics and antibody-based profiling. Mol Hum Reprod. 20(6):476–488. doi: 10.1093/molehr/gau018.
   PubMed Web of Science ®Google Scholar
• Dohle GR, Colpi GM, Hargreave TB, Papp GK, Jungwirth A, Weidner W, EAU Working Group on Male Infertility. 2005. EAU guidelines on male infertility. Eur Urol. 48(5):703–711. doi: 10.1016/j.eururo.2005.06.002.
   PubMed Web of Science ®Google Scholar
• Edelbrock MA, Kaliyaperumal S, Williams KJ. 2013. Structural, molecular and cellular functions of MSH2 and MSH6 during DNA mismatch repair, damage signaling and other noncanonical activities. Mutat Res. 743–744:53–66. doi: 10.1016/j.mrfmmm.2012.12.008.
   PubMed Web of Science ®Google Scholar
• Fainberg J, Hayden RP, Schlegel PN. 2019. Fertility management of Klinefelter syndrome. Expert Rev Endocrinol Metab. 14(6):369–380. doi: 10.1080/17446651.2019.1671821.
   PubMed Web of Science ®Google Scholar
• Gao Y, Wu H, Xu Y, Shen Q, Xu C, Geng H, Lv M, Tan Q, Li K, Tang D, et al. 2021. Novel biallelic mutations in SLC26A8 cause severe asthenozoospermia in humans owing to midpiece defects: insights into a putative dominant genetic disease. Hum Mutat. 43(3):434–443. doi: 10.1002/humu.24322.
   PubMed Web of Science ®Google Scholar
• Garrido N, Hervás I. 2020. Personalized medicine in infertile men. Urol Clin North Am. 47(2):245–255. doi: 10.1016/j.ucl.2019.12.011.
   PubMed Web of Science ®Google Scholar
• Gupta N, Sarkar S, Mehta P, Sankhwar SN, Rajender S. 2022. Polymorphisms in the HSF2, LRRC6, MEIG1 and PTIP genes correlate with sperm motility in idiopathic infertility. Andrologia. 54(9):e14517. doi: 10.1111/and.14517.
   PubMedGoogle Scholar
• Hall EA, Keighren M, Ford MJ, Davey T, Jarman AP, Smith LB, Jackson IJ, Mill P. 2013. Acute versus chronic loss of mammalian Azi1/Cep131 results in distinct ciliary phenotypes. PLoS Genet. 9(12):e1003928. doi: 10.1371/journal.pgen.1003928.
   PubMed Web of Science ®Google Scholar
• Hasin Y, Seldin M, Lusis A. 2017. Multi-omics approaches to disease. Genome Biol. 18(1):83. doi: 10.1186/s13059-017-1215-1.
   PubMed Web of Science ®Google Scholar
• Hodžić A, Maver A, Plaseska-Karanfilska D, Ristanović M, Noveski P, Zorn B, Terzic M, Kunej T, Peterlin B. 2021. De novo mutations in idiopathic male infertility—a pilot study. Andrology. 9(1):212–220. doi: 10.1111/andr.12897.
   PubMed Web of Science ®Google Scholar
• Houston BJ, Riera-Escamilla A, Wyrwoll MJ, Salas-Huetos A, Xavier MJ, Nagirnaja L, Friedrich C, Conrad DF, Aston KI, Krausz C, et al. 2021. A systematic review of the validated monogenic causes of human male infertility: 2020 update and a discussion of emerging gene–disease relationships. Hum Reprod Update. 28(1):15–29. doi: 10.1093/humupd/dmab030.
   PubMed Web of Science ®Google Scholar
• Hunter N, Borts RH. 1997. Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 11(12):1573–1582. doi: 10.1101/gad.11.12.1573.
   PubMed Web of Science ®Google Scholar
• Ito C, Makino T, Mutoh T, Kikkawa M, Toshimori K. 2023. The association of ODF4 with AK1 and AK2 in mice is essential for fertility through its contribution to flagellar shape. Sci Rep. 13(1):2969. doi: 10.1038/s41598-023-28177-z.
   PubMed Web of Science ®Google Scholar
• Jaillard S, McElreavy K, Robevska G, Akloul L, Ghieh F, Sreenivasan R, Beaumont M, Bashamboo A, Bignon-Topalovic J, Neyroud AS, et al. 2020. STAG3 homozygous missense variant causes primary ovarian insufficiency and male non-obstructive azoospermia. Mol Hum Reprod. 26(9):665–677. doi: 10.1093/molehr/gaaa050.
   PubMed Web of Science ®Google Scholar
• Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C, European Association of Urology Working Group on Male Infertility. 2012. European Association of Urology guidelines on Male Infertility: the 2012 update. Eur Urol. 62(2):324–332. doi: 10.1016/j.eururo.2012.04.048.
   PubMed Web of Science ®Google Scholar
• Khazaie Y, Nasr Esfahani MH. 2014. MicroRNA and male infertility: a potential for diagnosis. Int J Fertil Steril. 8(2):113–118.
   PubMedGoogle Scholar
• Konno A, Ikegami K, Konishi Y, Yang HJ, Abe M, Yamazaki M, Sakimura K, Yao I, Shiba K, Inaba K, et al. 2016. Ttll9–/– mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating. J Cell Sci. 129(14):2757–2766. doi: 10.1242/jcs.185983.
   PubMed Web of Science ®Google Scholar
• Krausz C, Escamilla AR, Chianese C. 2015. Genetics of male infertility: from research to clinic. Reproduction. 150(5):R159–R174. doi: 10.1530/REP-15-0261.
   PubMed Web of Science ®Google Scholar
• Krzastek SC, Farhi J, Gray M, Smith RP. 2020. Impact of environmental toxin exposure on male fertility potential. Transl Androl Urol. 9(6):2797–2813. doi: 10.21037/tau-20-685.
   PubMedGoogle Scholar
• Krzastek SC, Smith RP, Kovac JR. 2020. Future diagnostics in male infertility: genomics, epigenetics, metabolomics and proteomics. Transl Androl Urol. 9(Suppl. 2):S195–S205. doi: 10.21037/tau.2019.10.20.
   PubMedGoogle Scholar
• Kukurba KR, Montgomery SB. 2015. RNA sequencing and analysis. Cold Spring Harb Protoc. 2015(11):951–969. doi: 10.1101/pdb.top084970.
   PubMedGoogle Scholar
• Leaver RB. 2016. Male infertility: an overview of causes and treatment options. Br J Nurs. 25(18):S35–S40. doi: 10.12968/bjon.2016.25.18.S35.
   PubMedGoogle Scholar
• Lee VCY, Chow JFC, Yeung WSB, Ho PC. 2017. Preimplantation genetic diagnosis for monogenic diseases. Best Pract Res Clin Obstet Gynaecol. 44:68–75. doi: 10.1016/j.bpobgyn.2017.04.001.
   PubMed Web of Science ®Google Scholar
• Li P, Ji Z, Zhi E, Zhang Y, Han S, Zhao L, Tian R, Chen H, Huang Y, Zhang J, et al. 2022. Novel bi-allelic MSH4 variants causes meiotic arrest and non-obstructive azoospermia. Reprod Biol Endocrinol. 20(1):21. doi: 10.1186/s12958-022-00900-x.
   PubMed Web of Science ®Google Scholar
• Li W, Tang W, Teves ME, Zhang Z, Zhang L, Li H, Archer KJ, Peterson DL, Williams DC Jr, Strauss JF 3rd, et al. 2015. A MEIG1/PACRG complex in the manchette is essential for building the sperm flagella. Development. 142(5):921–930. doi: 10.1242/dev.119834.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang Y, Wen Y, Zhang T, Wang X, Jiang C, Zheng R, Zhou F, Chen D, Yang Y, et al. 2021. Whole-exome sequencing of a cohort of infertile men reveals novel causative genes in teratozoospermia that are chiefly related to sperm head defects. Hum Reprod. 37(1):152–177. doi: 10.1093/humrep/deab229.
   PubMed Web of Science ®Google Scholar
• Liu J, Rahim F, Zhou J, Fan S, Jiang H, Yu C, Chen J, Xu J, Yang G, Shah W, et al. 2023. Loss-of-function variants in KCTD19 cause non-obstructive azoospermia in humans. iScience. 26(7):107193. doi: 10.1016/j.isci.2023.107193.
   PubMed Web of Science ®Google Scholar
• Liu W, He X, Yang S, Zouari R, Wang J, Wu H, Kherraf ZE, Liu C, Coutton C, Zhao R, et al. 2019. Bi-allelic mutations in TTC21A induce asthenoteratospermia in humans and mice. Am J Hum Genet. 104(4):738–748. doi: 10.1016/j.ajhg.2019.02.020.
   PubMed Web of Science ®Google Scholar
• Liu X, Li Q, Wang W, Liu F. 2019. Aberrant expression of sperm‑specific glycolytic enzymes are associated with poor sperm quality. Mol Med Rep. 19(4):2471–2478. doi: 10.3892/mmr.2019.9926.
   PubMed Web of Science ®Google Scholar
• Liu XG, Hu HY, Guo YH, Sun YP. 2016. Correlation between Y chromosome microdeletion and male infertility. Genet Mol Res. 15(2). doi: 10.4238/gmr.15028426.
   Google Scholar
• Llavanera M, Delgado-Bermúdez A, Ribas-Maynou J, Salas-Huetos A, Yeste M. 2022. A systematic review identifying fertility biomarkers in semen: a clinical approach through omics to diagnose male infertility. Fertil Steril. 118(2):291–313. doi: 10.1016/j.fertnstert.2022.04.028.
   PubMed Web of Science ®Google Scholar
• Lundy SD, Sangwan N, Parekh NV, Selvam MKP, Gupta S, McCaffrey P, Bessoff K, Vala A, Agarwal A, Sabanegh ES, et al. 2021. Functional and taxonomic dysbiosis of the gut, urine, and semen microbiomes in male infertility. Eur Urol. 79(6):826–836. doi: 10.1016/j.eururo.2021.01.014.
   PubMed Web of Science ®Google Scholar
• Lutzmann M, Grey C, Traver S, Ganier O, Maya-Mendoza A, Ranisavljevic N, Bernex F, Nishiyama A, Montel N, Gavois E, et al. 2012. MCM8- and MCM9-deficient mice reveal gametogenesis defects and genome instability due to impaired homologous recombination. Mol Cell. 47(4):523–534. doi: 10.1016/j.molcel.2012.05.048.
   PubMed Web of Science ®Google Scholar
• Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. 2013. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLOS One. 8(1):e55387. doi: 10.1371/journal.pone.0055387.
   PubMed Web of Science ®Google Scholar
• Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. 2008. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18(9):1509–1517. doi: 10.1101/gr.079558.108.
   PubMed Web of Science ®Google Scholar
• Martinez G, Coutton C, Loeuillet C, Cazin C, Muroňová J, Boguenet M, Lambert E, Dhellemmes M, Chevalier G, Hograindleur JP, et al. 2022. Oligogenic heterozygous inheritance of sperm abnormalities in mouse. Elife. 11:e75373. doi: 10.7554/eLife.75373.
   PubMed Web of Science ®Google Scholar
• Mikec Š, Kolenc Ž, Peterlin B, Horvat S, Pogorevc N, Kunej T. 2022. Syndromic male subfertility: a network view of genome–phenome associations. Andrology. 10(4):720–732. doi: 10.1111/andr.13167.
   PubMed Web of Science ®Google Scholar
• Mikeska T, Craig JM. 2014. DNA methylation biomarkers: cancer and beyond. Genes. 5(3):821–864. doi: 10.3390/genes5030821.
   PubMed Web of Science ®Google Scholar
• Misra BB, Langefeld CD, Olivier M, Cox LA. 2018. Integrated omics: tools, advances, and future approaches. J Mol Endocrinol. doi: 10.1530/JME-18-0055.
   Google Scholar
• Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6(7):e1000097. doi: 10.1371/journal.pmed.1000097.
   PubMed Web of Science ®Google Scholar
• Ning M, Lo EH. 2010. Opportunities and challenges in omics. Transl Stroke Res. 1(4):233–237. doi: 10.1007/s12975-010-0048-y.
   PubMed Web of Science ®Google Scholar
• Omolaoye TS, Omolaoye VA, Kandasamy RK, Hachim MY, Du Plessis SS. 2022. Omics and Male Infertility: highlighting the application of transcriptomic data. Life. 12(2):280. doi: 10.3390/life12020280.
   PubMedGoogle Scholar
• Oud MS, Smits RM, Smith HE, Mastrorosa FK, Holt GS, Houston BJ, de Vries PF, Alobaidi BKS, Batty LE, Ismail H, et al. 2022. A de novo paradigm for male infertility. Nat Commun. 13(1):154. doi: 10.1038/s41467-021-27132-8.
   PubMed Web of Science ®Google Scholar
• Peterlin A, Kunej T, Peterlin B. 2019. The role of circadian rhythm in male reproduction. Curr Opin Endocrinol Diabetes Obes. 26(6):313–316. doi: 10.1097/MED.0000000000000512.
   PubMedGoogle Scholar
• Pirih N, Kunej T. 2017. Toward a taxonomy for multi-omics science? Terminology development for whole genome study approaches by omics technology and hierarchy. OMICS. 21(1):1–16. doi: 10.1089/omi.2016.0144.
   PubMed Web of Science ®Google Scholar
• Punab M, Poolamets O, Paju P, Vihljajev V, Pomm K, Ladva R, Korrovits P, Laan M. 2017. Causes of male infertility: a 9-year prospective monocentre study on 1737 patients with reduced total sperm counts. Hum Reprod. 32(1):18–31. doi: 10.1093/humrep/dew284.
   PubMed Web of Science ®Google Scholar
• Rastgar Rezaei Y, Zarezadeh R, Nikanfar S, Oghbaei H, Nazdikbin N, Bahrami-Asl Z, Zarghami N, Ahmadi Y, Fattahi A, Nouri M, et al. 2021. microRNAs in the pathogenesis of non-obstructive azoospermia: the underlying mechanisms and therapeutic potentials. Syst Biol Reprod Med. 67(5):337–353. doi: 10.1080/19396368.2021.1951890.
   PubMed Web of Science ®Google Scholar
• Seal RL, Braschi B, Gray K, Jones TEM, Tweedie S, Haim-Vilmovsky L, Bruford EA. 2023. Genenames.org: the HGNC resources in 2023. Nucleic Acids Res. 51(D1):D1003–D1009. doi: 10.1093/nar/gkac888.
   PubMed Web of Science ®Google Scholar
• Seal RL, Chen LL, Griffiths-Jones S, Lowe TM, Mathews MB, O'Reilly D, Pierce AJ, Stadler PF, Ulitsky I, Wolin SL, et al. 2020. A guide to naming human non-coding RNA genes. EMBO J. 39(6):e103777. doi: 10.15252/embj.2019103777.
   PubMed Web of Science ®Google Scholar
• Sha Y, Liu W, Nie H, Han L, Ma C, Zhang X, Xiao Z, Qin W, Jiang X, Wei X. 2022. Homozygous mutation in DNALI1 leads to asthenoteratozoospermia by affecting the inner dynein arms. Front Endocrinol. 13:1058651. doi: 10.3389/fendo.2022.1058651.
   PubMed Web of Science ®Google Scholar
• Sha YW, Sha YK, Ji ZY, Mei LB, Ding L, Zhang Q, Qiu PP, Lin SB, Wang X, Li P, et al. 2018. TSGA10 is a novel candidate gene associated with acephalic spermatozoa. Clin Genet. 93(4):776–783. doi: 10.1111/cge.13140.
   PubMed Web of Science ®Google Scholar
• Shen Y, Zhang F, Li F, Jiang X, Yang Y, Li X, Li W, Wang X, Cheng J, Liu M, et al. 2019. Loss-of-function mutations in QRICH2 cause male infertility with multiple morphological abnormalities of the sperm flagella. Nat Commun. 10(1):433. doi: 10.1038/s41467-018-08182-x.
   PubMedGoogle Scholar
• Silber SJ, Repping S. 2002. Transmission of male infertility to future generations: lessons from the Y chromosome. Hum Reprod Update. 8(3):217–229. doi: 10.1093/humupd/8.3.217.
   PubMed Web of Science ®Google Scholar
• Sobotka V, Vozdova M, Heracek J, Rubes J. 2015. A rare Robertsonian translocation rob(14;22) carrier with azoospermia, meiotic defects, and testicular sperm aneuploidy. Syst Biol Reprod Med. 61(4):245–250. doi: 10.3109/19396368.2015.1045089.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. 2019. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47(D1):D607–D613. doi: 10.1093/nar/gky1131.
   PubMed Web of Science ®Google Scholar
• Tenenbaum-Rakover Y, Weinberg-Shukron A, Renbaum P, Lobel O, Eideh H, Gulsuner S, Dahary D, Abu-Rayyan A, Kanaan M, Levy-Lahad E, et al. 2015. Minichromosome maintenance complex component 8 (MCM8) gene mutations result in primary gonadal failure. J Med Genet. 52(6):391–399. doi: 10.1136/jmedgenet-2014-102921.
   PubMed Web of Science ®Google Scholar
• Tu C, Nie H, Meng L, Yuan S, He W, Luo A, Li H, Li W, Du J, Lu G, et al. 2019. Identification of DNAH6 mutations in infertile men with multiple morphological abnormalities of the sperm flagella. Sci Rep. 9(1):15864. doi: 10.1038/s41598-019-52436-7.
   PubMedGoogle Scholar
• Wagner AO, Turk A, Kunej T. 2023. Towards a multi-omics of male infertility. World J Mens Health. 41(2):272–288. doi: 10.5534/wjmh.220186.
   PubMedGoogle Scholar
• Wang M, Yang QY, Zhou JP, Tan HP, Hu J, Jin L, Zhu LX. 2023. Novel compound heterozygous mutations in DNAH1 cause primary infertility in Han Chinese males with multiple morphological abnormalities of the sperm flagella. Asian J Androl. 25(4):512–519. doi: 10.4103/aja202292.
   PubMed Web of Science ®Google Scholar
• Wei X, Sha Y, Wei Z, Zhu X, He F, Zhang X, Liu W, Wang Y, Lu Z. 2021. Bi-allelic mutations in DNAH7 cause asthenozoospermia by impairing the integrality of axoneme structure. Acta Biochim Biophys Sin. 53(10):1300–1309. doi: 10.1093/abbs/gmab113.
   Google Scholar
• Wistuba J, Mittag J, Luetjens CM, Cooper TG, Yeung CH, Nieschlag E, Bauer K. 2007. Male congenital hypothyroid 2007. Pax8–/– mice are infertile despite adequate treatment with thyroid hormone. J Endocrinol. 192(1):99–109. doi: 10.1677/JOE-06-0054.
   PubMed Web of Science ®Google Scholar
• Wu H, Liu Y, Li Y, Li K, Xu C, Gao Y, Lv M, Guo R, Xu Y, Zhou P, et al. 2023. DNALI1 deficiency causes male infertility with severe asthenozoospermia in humans and mice by disrupting the assembly of the flagellar inner dynein arms and fibrous sheath. Cell Death Dis. 14(2):127. doi: 10.1038/s41419-023-05653-y.
   PubMed Web of Science ®Google Scholar
• Xie Z, Bailey A, Kuleshov MV, Clarke DJB, Evangelista JE, Jenkins SL, Lachmann A, Wojciechowicz ML, Kropiwnicki E, Jagodnik KM, et al. 2021. Gene set knowledge discovery with Enrichr. Curr Protoc. 1(3):e90. doi: 10.1002/cpz1.90.
   PubMedGoogle Scholar
• Xu X, Sha YW, Mei LB, Ji ZY, Qiu PP, Ji H, Li P, Wang T, Li L. 2018. A familial study of twins with severe asthenozoospermia identified a homozygous SPAG17 mutation by whole-exome sequencing. Clin Genet. 93(2):345–349. doi: 10.1111/cge.13059.
   PubMed Web of Science ®Google Scholar
• Yap YT, Li W, Huang Q, Zhou Q, Zhang D, Sheng Y, Mladenovic-Lucas L, Yee SP, Orwig KE, Granneman JG, et al. 2023. DNALI1 interacts with the MEIG1/PACRG complex within the manchette and is required for proper sperm flagellum assembly in mice. Elife. 12:e79620. doi: 10.7554/eLife.79620.
   PubMed Web of Science ®Google Scholar
• Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, Sullivan E, Vanderpoel S, International Committee for Monitoring Assisted Reproductive Technology; World Health Organization. 2009. International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil Steril. 92(5):1520–1524. doi: 10.1016/j.fertnstert.2009.09.009.
   PubMed Web of Science ®Google Scholar
• Zhang J, Mu X, Xia Y, Martin FL, Hang W, Liu L, Tian M, Huang Q, Shen H. 2014. Metabolomic analysis reveals a unique urinary pattern in normozoospermic infertile men. J Proteome Res. 13(6):3088–3099. doi: 10.1021/pr5003142.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Shen X, Gude DR, Wilkinson BM, Justice MJ, Flickinger CJ, Herr JC, Eddy EM, Strauss JF 3rd. 2009. MEIG1 is essential for spermiogenesis in mice. Proc Natl Acad Sci U S A. 106(40):17055–17060. doi: 10.1073/pnas.0906414106.
   PubMed Web of Science ®Google Scholar
• Zupanic A, Bernstein HC, Heiland I. 2020. Systems biology: current status and challenges. Cell Mol Life Sci. 77(3):379–380. doi: 10.1007/s00018-019-03410-z.
   PubMed Web of Science ®Google Scholar