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Vertebrate reproductive science and technology
RESEARCH ARTICLE

IQ motif containing D (IQCD), a new acrosomal protein involved in the acrosome reaction and fertilisation

Peng Zhang https://orcid.org/0000-0002-8035-9798 A , Wanjun Jiang A , Na Luo A , Wenbing Zhu A B and Liqing Fan A B C
+ Author Affiliations
- Author Affiliations

A Institute of Reproductive and Stem Cell Engineering, School of Basic Medicine, Central South University, Xiangya Road 88#, Changsha, Hunan Province, 410078, the People’s Republic of China.

B Reproductive and Genetic Hospital of CITIC – Xiangya, Xiangya Road 84#, Changsha, Hunan Province, 410078, the People’s Republic of China.

C Corresponding author. Email: liqingfan@csu.edu.cn

Reproduction, Fertility and Development 31(5) 898-914 https://doi.org/10.1071/RD18416
Submitted: 25 July 2018  Accepted: 7 December 2018   Published: 4 February 2019

Abstract

The acrosome is single, large, dense-core secretory granule overlying the nucleus of most mammalian spermatozoa. Its exocytosis, the acrosome reaction, is a crucial event during fertilisation. In this study we identified a new acrosome-associated gene, namely IQ motif containing D (IQCD), expressed nearly in multiple tissues with highest expression levels in the testis. In mouse testis, Iqcd transcript accumulated from Postnatal Day (PND) 1 to adulthood. However, expression of IQCD protein at the testicular development stage started primarily from PND 18 and increased in an age-dependent manner until plateauing in adulthood. IQCD was primarily accumulated in the acrosome area of round and elongating spermatids within seminiferous tubules of the testes during the late stage of spermiogenesis; this immunolocalisation pattern is similar in mice and humans. IQCD levels in spermatozoa were significantly lower in IVF patients with total fertilisation failure or a low fertilisation rate than in healthy men. Anti-IQCD antibody significantly inhibited the acrosome reaction and slightly reduced protein tyrosine phosphorylation levels in human spermatozoa, but specifically blocked murine IVF. IQCD interacted with mammalian homolog of C. elegans uncoordinated gene 13 (Munc13) in spermatozoa and may participate in acrosome exocytosis. In conclusion, this study identified a new acrosomal protein, namely IQCD, which is involved in fertilisation and the acrosome reaction.

Additional keyword: spermatid.


References

Awata, J., Song, K., Lin, J., King, S. M., Sanderson, M. J., Nicastro, D., and Witman, G. B. (2015). DRC3 connects the N-DRC to dynein g to regulate flagellar waveform. Mol. Biol. Cell 26, 2788–2800.
DRC3 connects the N-DRC to dynein g to regulate flagellar waveform.Crossref | GoogleScholarGoogle Scholar | 26063732PubMed |

Bähler, M., and Rhoads, A. (2002). Calmodulin signaling via the IQ motif. FEBS Lett. 513, 107–113.
Calmodulin signaling via the IQ motif.Crossref | GoogleScholarGoogle Scholar | 11911888PubMed |

Barbelanne, M., Hossain, D., Chan, D. P., Peranen, J., and Tsang, W. Y. (2015). Nephrocystin proteins NPHP5 and Cep290 regulate BBSome integrity, ciliary trafficking and cargo delivery. Hum. Mol. Genet. 24, 2185–2200.
Nephrocystin proteins NPHP5 and Cep290 regulate BBSome integrity, ciliary trafficking and cargo delivery.Crossref | GoogleScholarGoogle Scholar | 25552655PubMed |

Bell, R., Hubbard, A., Chettier, R., Chen, D., Miller, J. P., Kapahi, P., Tarnopolsky, M., Sahasrabuhde, S., Melov, S., and Hughes, R. E. (2009). A human protein interaction network shows conservation of aging processes between human and invertebrate species. PLoS Genet. 5, e1000414.
A human protein interaction network shows conservation of aging processes between human and invertebrate species.Crossref | GoogleScholarGoogle Scholar | 19293945PubMed |

Bello, O. D., Zanetti, M. N., Mayorga, L. S., and Michaut, M. A. (2012). RIM, Munc13, and Rab3A interplay in acrosomal exocytosis. Exp. Cell Res. 318, 478–488.
RIM, Munc13, and Rab3A interplay in acrosomal exocytosis.Crossref | GoogleScholarGoogle Scholar | 22248876PubMed |

Bellvé, A. R., Cavicchia, J. C., Millette, C. F., O’Brien, D. A., Bhatnagar, Y. M., and Dym, M. (1977). Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74, 68–85.
Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization.Crossref | GoogleScholarGoogle Scholar | 874003PubMed |

Bower, R., Tritschler, D., Vanderwaal, K., Perrone, C. A., Mueller, J., Fox, L., Sale, W. S., and Porter, M. E. (2013). The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes. Mol. Biol. Cell 24, 1134–1152.
The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes.Crossref | GoogleScholarGoogle Scholar | 23427265PubMed |

Bower, R., Tritschler, D., Mills, K. V., Heuser, T., Nicastro, D., and Porter, M. E. (2018). DRC2/CCDC65 is a central hub for assembly of the nexin–dynein regulatory complex and other regulators of ciliary and flagellar motility. Mol. Biol. Cell 29, 137–153.
DRC2/CCDC65 is a central hub for assembly of the nexin–dynein regulatory complex and other regulators of ciliary and flagellar motility.Crossref | GoogleScholarGoogle Scholar | 29167384PubMed |

Castaneda, J. M., Hua, R., Miyata, H., Oji, A., Guo, Y., Cheng, Y., Zhou, T., Guo, X., Cui, Y., Shen, B., Wang, Z., Hu, Z., Zhou, Z., Sha, J., Prunskaite-Hyyrylainen, R., Yu, Z., Ramirez-Solis, R., Ikawa, M., Matzuk, M. M., and Liu, M. (2017). TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa. Proc. Natl Acad. Sci. USA 114, E5370–E5378.
TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 28630322PubMed |

Chen, L. T., Liang, W. X., Chen, S., Li, R. K., Tan, J. L., Xu, P. F., Luo, L. F., Wang, L., Yu, S. H., Meng, G., Li, K. K., Liu, T. X., Chen, Z., and Chen, S. J. (2014). Functional and molecular features of the calmodulin-interacting protein IQCG required for haematopoiesis in zebrafish. Nat. Commun. 5, 3811.
Functional and molecular features of the calmodulin-interacting protein IQCG required for haematopoiesis in zebrafish.Crossref | GoogleScholarGoogle Scholar | 24787902PubMed |

Choi, D., Lee, E., Hwang, S., Jun, K., Kim, D., Yoon, B. K., Shin, H. S., and Lee, J. H. (2001). The biological significance of phospholipase C beta 1 gene mutation in mouse sperm in the acrosome reaction, fertilization, and embryo development. J. Assist. Reprod. Genet. 18, 305–310.
The biological significance of phospholipase C beta 1 gene mutation in mouse sperm in the acrosome reaction, fertilization, and embryo development.Crossref | GoogleScholarGoogle Scholar | 11464583PubMed |

De Kretser, D. M., and Baker, H. W. (1999). Infertility in men: recent advances and continuing controversies. J. Clin. Endocrinol. Metab. 84, 3443–3450.
| 10522977PubMed |

Dimova, K., Kalkhof, S., Pottratz, I., Ihling, C., Rodriguez-Castaneda, F., Liepold, T., Griesinger, C., Brose, N., Sinz, A., and Jahn, O. (2009). Structural insights into the calmodulin–Munc13 interaction obtained by cross-linking and mass spectrometry. Biochemistry 48, 5908–5921.
Structural insights into the calmodulin–Munc13 interaction obtained by cross-linking and mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 19492809PubMed |

Fang, P., Xu, W., Li, D., Zhao, X., Dai, J., Wang, Z., Yan, X., Qin, M., Zhang, Y., Xu, C., Wang, L., and Qiao, Z. (2015). A novel acrosomal protein, IQCF1, involved in sperm capacitation and the acrosome reaction. Andrology 3, 332–344.
A novel acrosomal protein, IQCF1, involved in sperm capacitation and the acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 25380116PubMed |

Geng, Q., Ni, L., Ouyang, B., Hu, Y., Zhao, Y., and Guo, J. (2016). A novel testis-specific gene, Ccdc136, is required for acrosome formation and fertilization in mice. Reprod. Sci. 23, 1387–1396.
A novel testis-specific gene, Ccdc136, is required for acrosome formation and fertilization in mice.Crossref | GoogleScholarGoogle Scholar | 27076447PubMed |

Gou, L. T., Kang, J. Y., Dai, P., Wang, X., Li, F., Zhao, S., Zhang, M., Hua, M. M., Lu, Y., Zhu, Y., Li, Z., Chen, H., Wu, L. G., Li, D., Fu, X. D., Li, J., Shi, H. J., and Liu, M. F. (2017). Ubiquitination-deficient mutations in human Piwi cause male infertility by impairing histone-to-protamine exchange during spermiogenesis. Cell 169, 1090–1104.e13.
Ubiquitination-deficient mutations in human Piwi cause male infertility by impairing histone-to-protamine exchange during spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 28552346PubMed |

Guo, R., Ma, P. P., Ma, J., Ge, Y. H., Xue, S. P., and Han, D. S. (2004). Cloning and characterization of a novel gene SRG-L expressed in late stages of mouse spermatogenic cells. Acta Biochim. Biophys. Sin. (Shanghai) 36, 315–322.
Cloning and characterization of a novel gene SRG-L expressed in late stages of mouse spermatogenic cells.Crossref | GoogleScholarGoogle Scholar | 15156272PubMed |

Gupta, M. K., Jayaram, S., Madugundu, A. K., Chavan, S., Advani, J., Pandey, A., Thongboonkerd, V., and Sirdeshmukh, R. (2014). Chromosome-centric human proteome project: deciphering proteins associated with glioma and neurodegenerative disorders on chromosome 12. J. Proteome Res. 13, 3178–3190.
Chromosome-centric human proteome project: deciphering proteins associated with glioma and neurodegenerative disorders on chromosome 12.Crossref | GoogleScholarGoogle Scholar | 24804578PubMed |

Gurkan, H., Tozkir, H., Goncu, E., Ulusal, S., and Yazar, M. (2015). The relationship between methylenetetrahydrofolate reductase c.677TT genotype and oligozoospermia in infertile male patients living in the Trakya region of Turkey. Andrologia 47, 1068–1074.
The relationship between methylenetetrahydrofolate reductase c.677TT genotype and oligozoospermia in infertile male patients living in the Trakya region of Turkey.Crossref | GoogleScholarGoogle Scholar | 25428700PubMed |

Hamamah, S., Anahory, T., Ferriere, A., Loup, V., Reyftmann, L., and Dechaud, H. (2009). [Therapeutic solutions for male infertility.] J. Gynecol. Obstet. Biol. Reprod. (Paris) 38, F58–F64.
[Therapeutic solutions for male infertility.]Crossref | GoogleScholarGoogle Scholar |

Harris, T. P., Schimenti, K. J., Munroe, R. J., and Schimenti, J. C. (2014). IQ motif-containing G (Iqcg) is required for mouse spermiogenesis. G3 (Bethesda) 4, 367–372.
IQ motif-containing G (Iqcg) is required for mouse spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 24362311PubMed |

Horani, A., Brody, S. L., Ferkol, T. W., Shoseyov, D., Wasserman, M. G., Ta-shma, A., Wilson, K. S., Bayly, P. V., Amirav, I., Cohen-Cymberknoh, M., Dutcher, S. K., Elpeleg, O., and Kerem, E. (2013). CCDC65 mutation causes primary ciliary dyskinesia with normal ultrastructure and hyperkinetic cilia. PLoS One 8, e72299.
CCDC65 mutation causes primary ciliary dyskinesia with normal ultrastructure and hyperkinetic cilia.Crossref | GoogleScholarGoogle Scholar | 23991085PubMed |

Inaba, K. (2007). Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects. Ann. N. Y. Acad. Sci. 1101, 506–526.
Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects.Crossref | GoogleScholarGoogle Scholar | 17363437PubMed |

Jeanson, L., Thomas, L., Copin, B., Coste, A., Sermet-Gaudelus, I., Dastot-Le Moal, F., Duquesnoy, P., Montantin, G., Collot, N., Tissier, S., Papon, J. F., Clement, A., Louis, B., Escudier, E., Amselem, S., and Legendre, M. (2016). Mutations in GAS8, a gene encoding a nexin–dynein regulatory complex subunit, cause primary ciliary dyskinesia with axonemal disorganization. Hum. Mutat. 37, 776–785.
Mutations in GAS8, a gene encoding a nexin–dynein regulatory complex subunit, cause primary ciliary dyskinesia with axonemal disorganization.Crossref | GoogleScholarGoogle Scholar | 27120127PubMed |

Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275–282.
| 1633570PubMed |

Juneja, R., Agulnik, S. I., and Silver, L. M. (1998). Sequence divergence within the sperm-specific polypeptide TCTE1 is correlated with species-specific differences in sperm binding to zona-intact eggs. J. Androl. 19, 183–188.
| 9570741PubMed |

Kawamoto, A., Ohashi, K., Kishikawa, H., Zhu, L. Q., Azuma, C., and Murata, Y. (1999). Two-color fluorescence staining of lectin and anti-CD46 antibody to assess acrosomal status. Fertil. Steril. 71, 497–501.
Two-color fluorescence staining of lectin and anti-CD46 antibody to assess acrosomal status.Crossref | GoogleScholarGoogle Scholar | 10065788PubMed |

Khatun, A., Rahman, M. S., and Pang, M. G. (2018). Clinical assessment of the male fertility. Obstet. Gynecol. Sci. 61, 179–191.
Clinical assessment of the male fertility.Crossref | GoogleScholarGoogle Scholar | 29564308PubMed |

Klinovska, K., Sebkova, N., and Dvorakova-Hortova, K. (2014). Sperm-egg fusion: a molecular enigma of mammalian reproduction. Int. J. Mol. Sci. 15, 10652–10868.
Sperm-egg fusion: a molecular enigma of mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 24933635PubMed |

Kim, M. A., and Sohn, Y. C. (2017). Characterization of a sea urchin IQ motif containing protein D as a coactivator of nuclear receptors. Zool. Sci. 34, 235–241.
Characterization of a sea urchin IQ motif containing protein D as a coactivator of nuclear receptors.Crossref | GoogleScholarGoogle Scholar | 28589840PubMed |

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Leung, C. S., Yeung, T. L., Yip, K. P., Pradeep, S., Balasubramanian, L., Liu, J., Wong, K. K., Mangala, L. S., Armaiz-Pena, G. N., Lopez-Berestein, G., Sood, A. K., Birrer, M. J., and Mok, S. C. (2014). Calcium-dependent FAK/CREB/TNNC1 signalling mediates the effect of stromal MFAP5 on ovarian cancer metastatic potential. Nat. Commun. 5, 5092.
Calcium-dependent FAK/CREB/TNNC1 signalling mediates the effect of stromal MFAP5 on ovarian cancer metastatic potential.Crossref | GoogleScholarGoogle Scholar | 25277212PubMed |

Li, W., Ma, C., Guan, R., Xu, Y., Tomchick, D. R., and Rizo, J. (2011). The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors. Structure 19, 1443–1455.
The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors.Crossref | GoogleScholarGoogle Scholar | 22000513PubMed |

Li, R. K., Tan, J. L., Chen, L. T., Feng, J. S., Liang, W. X., Guo, X. J., Liu, P., Chen, Z., Sha, J. H., Wang, Y. F., and Chen, S. J. (2014). Iqcg is essential for sperm flagellum formation in mice. PLoS One 9, e98053.
Iqcg is essential for sperm flagellum formation in mice.Crossref | GoogleScholarGoogle Scholar | 25393402PubMed |

Li, Y., Lin, S., Luo, M., Guo, H., Chen, J., Ma, Q., Gu, Y., Jiang, Z., and Gui, Y. (2015). FAM170B, a novel acrosomal protein involved in fertilization in mice. Mol. Reprod. Dev. 82, 787–796.
FAM170B, a novel acrosomal protein involved in fertilization in mice.Crossref | GoogleScholarGoogle Scholar | 26179146PubMed |

Lindsay, T. J., and Vitrikas, K. R. (2015). Evaluation and treatment of infertility. Am. Fam. Physician 91, 308–314.
| 25822387PubMed |

Lipstein, N., Sakaba, T., Cooper, B. H., Lin, K. H., Strenzke, N., Ashery, U., Rhee, J. S., Taschenberger, H., Neher, E., and Brose, N. (2013). Dynamic control of synaptic vesicle replenishment and short-term plasticity by Ca(2+)–calmodulin–Munc13-1 signaling. Neuron 79, 82–96.
Dynamic control of synaptic vesicle replenishment and short-term plasticity by Ca(2+)–calmodulin–Munc13-1 signaling.Crossref | GoogleScholarGoogle Scholar | 23770256PubMed |

Liu, J., Wu, Y., Xu, S., Su, D., Han, Y., and Wu, X. (2017). Retrospective evaluation of pregnancy outcomes and clinical implications of 34 Han Chinese women with unicornuate uterus who received IVF-ET or ICSI-ET treatment. J. Obstet. Gynaecol. 37, 1020–1024.
Retrospective evaluation of pregnancy outcomes and clinical implications of 34 Han Chinese women with unicornuate uterus who received IVF-ET or ICSI-ET treatment.Crossref | GoogleScholarGoogle Scholar | 28657383PubMed |

Ma, Q., Wang, H., Guo, R., Wang, H., Ge, Y., Ma, J., Xue, S., and Han, D. (2006). Molecular cloning and characterization of SRG-L, a novel mouse gene developmentally expressed in spermatogenic cells. Mol. Reprod. Dev. 73, 1075–1083.
Molecular cloning and characterization of SRG-L, a novel mouse gene developmentally expressed in spermatogenic cells.Crossref | GoogleScholarGoogle Scholar | 16804880PubMed |

Ma, C., Li, W., Xu, Y., and Rizo, J. (2011). Munc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex. Nat. Struct. Mol. Biol. 18, 542–549.
Munc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex.Crossref | GoogleScholarGoogle Scholar | 21499244PubMed |

Ma, D. D., Pan, M. Y., Hou, C. C., Tan, F. Q., and Yang, W. X. (2017). KIFC1 and myosin VA: two motors for acrosomal biogenesis and nuclear shaping during spermiogenesis of Portunus trituberculatus. Cell Tissue Res. 369, 625–640.
KIFC1 and myosin VA: two motors for acrosomal biogenesis and nuclear shaping during spermiogenesis of Portunus trituberculatus.Crossref | GoogleScholarGoogle Scholar | 28639134PubMed |

Nagdas, S. K., Smith, L., Medina-Ortiz, I., Hernandez-Encarnacion, L., and Raychoudhury, S. (2016). Identification of bovine sperm acrosomal proteins that interact with a 32-kDa acrosomal matrix protein. Mol. Cell. Biochem. 414, 153–169.
Identification of bovine sperm acrosomal proteins that interact with a 32-kDa acrosomal matrix protein.Crossref | GoogleScholarGoogle Scholar | 26897631PubMed |

Nishimune, Y., and Tanaka, H. (2006). Infertility caused by polymorphisms or mutations in spermatogenesis-specific genes. J. Androl. 27, 326–334.
Infertility caused by polymorphisms or mutations in spermatogenesis-specific genes.Crossref | GoogleScholarGoogle Scholar | 16474012PubMed |

Nishio, S., and Matsuda, T. (2017). Fertilization 1: sperm–egg interaction. Adv. Exp. Med. Biol. 1001, 91–103.
Fertilization 1: sperm–egg interaction.Crossref | GoogleScholarGoogle Scholar | 28980231PubMed |

Oda, T., Yanagisawa, H., and Kikkawa, M. (2015). Detailed structural and biochemical characterization of the nexin–dynein regulatory complex. Mol. Biol. Cell 26, 294–304.
Detailed structural and biochemical characterization of the nexin–dynein regulatory complex.Crossref | GoogleScholarGoogle Scholar | 25411337PubMed |

Paiardi, C., Pasini, M. E., Gioria, M., and Berruti, G. (2011). Failure of acrosome formation and globozoospermia in the wobbler mouse, a Vps54 spontaneous recessive mutant. Spermatogenesis 1, 52–62.
Failure of acrosome formation and globozoospermia in the wobbler mouse, a Vps54 spontaneous recessive mutant.Crossref | GoogleScholarGoogle Scholar | 21866276PubMed |

Rittmeyer, E. N., Daniel, S., Hsu, S. C., and Osman, M. A. (2008). A dual role for IQGAP1 in regulating exocytosis. J. Cell Sci. 121, 391–403.
A dual role for IQGAP1 in regulating exocytosis.Crossref | GoogleScholarGoogle Scholar | 18216334PubMed |

Schietroma, C., Yu, H. Y., Wagner, M. C., Umbach, J. A., Bement, W. M., and Gundersen, C. B. (2007). A role for myosin 1e in cortical granule exocytosis in Xenopus oocytes. J. Biol. Chem. 282, 29504–29513.
A role for myosin 1e in cortical granule exocytosis in Xenopus oocytes.Crossref | GoogleScholarGoogle Scholar | 17702742PubMed |

Sokal, I., and Haeseleer, F. (2011). Insight into the role of Ca2+-binding protein 5 in vesicle exocytosis. Invest. Ophthalmol. Vis. Sci. 52, 9131–9141.
Insight into the role of Ca2+-binding protein 5 in vesicle exocytosis.Crossref | GoogleScholarGoogle Scholar | 22039235PubMed |

Suryavathi, V., Panneerdoss, S., Wolkowicz, M. J., Shetty, J., Sherman, N. E., Flickinger, C. J., and Herr, J. C. (2015). Dynamic changes in equatorial segment protein 1 (SPESP1) glycosylation during mouse spermiogenesis. Biol. Reprod. 92, 129.
Dynamic changes in equatorial segment protein 1 (SPESP1) glycosylation during mouse spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 25761597PubMed |

Watanabe, M., Nomura, K., Ohyama, A., Ishikawa, R., Komiya, Y., Hosaka, K., Yamauchi, E., Taniguchi, H., Sasakawa, N., Kumakura, K., Ushiki, T., Sato, O., Ikebe, M., and Igarashi, M. (2005). Myosin-VA regulates exocytosis through the submicromolar Ca2+-dependent binding of syntaxin-1A. Mol. Biol. Cell 16, 4519–4530.
Myosin-VA regulates exocytosis through the submicromolar Ca2+-dependent binding of syntaxin-1A.Crossref | GoogleScholarGoogle Scholar | 16030255PubMed |

Wirschell, M., Olbrich, H., Werner, C., Tritschler, D., Bower, R., Sale, W. S., Loges, N. T., Pennekamp, P., Lindberg, S., Stenram, U., Carlen, B., Horak, E., Kohler, G., Nurnberg, P., Nurnberg, G., Porter, M. E., and Omran, H. (2013). The nexin–dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nat. Genet. 45, 262–268.
The nexin–dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans.Crossref | GoogleScholarGoogle Scholar | 23354437PubMed |

Yang, Y., Cochran, D. A., Gargano, M. D., King, I., Samhat, N. K., Burger, B. P., Sabourin, K. R., Hou, Y., Awata, J., Parry, D. A., Marshall, W. F., Witman, G. B., and Lu, X. (2011). Regulation of flagellar motility by the conserved flagellar protein CG34110/Ccdc135/FAP50. Mol. Biol. Cell 22, 976–987.
Regulation of flagellar motility by the conserved flagellar protein CG34110/Ccdc135/FAP50.Crossref | GoogleScholarGoogle Scholar | 21289096PubMed |

Yeh, S. D., Chen, Y. J., Chang, A. C., Ray, R., She, B. R., Lee, W. S., Chiang, H. S., Cohen, S. N., and Lin-Chao, S. (2002). Isolation and properties of Gas8, a growth arrest-specific gene regulated during male gametogenesis to produce a protein associated with the sperm motility apparatus. J. Biol. Chem. 277, 6311–6317.
Isolation and properties of Gas8, a growth arrest-specific gene regulated during male gametogenesis to produce a protein associated with the sperm motility apparatus.Crossref | GoogleScholarGoogle Scholar | 11751847PubMed |

Zhang, J., Ding, X., Bian, Z., Xia, Y., Lu, C., Wang, S., Song, L., and Wang, X. (2010). The effect of anti-eppin antibodies on ionophore A23187-induced calcium influx and acrosome reaction of human spermatozoa. Hum. Reprod. 25, 29–36.
The effect of anti-eppin antibodies on ionophore A23187-induced calcium influx and acrosome reaction of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 19801569PubMed |

Zheng, Y., Zhang, J., Wang, L., Zhou, Z., Xu, M., Li, J., and Sha, J. H. (2006). Cloning and characterization of a novel sperm tail protein, NYD-SP28. Int. J. Mol. Med. 18, 1119–1125.
| 17089017PubMed |