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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Spermatogenic phenotype of testis-specific protein, Y-encoded, 1 (TSPY1) dosage deficiency is independent of variations in TSPY-like 1 (TSPYL1) and TSPY-like 5 (TSPYL5): a case-control study in a Han Chinese population

Xiling Yang A , Xiangyou Leng A , Wenling Tu A , Yunqiang Liu A , Jinyan Xu A , Xue Pei A , Yongyi Ma B , Dong Yang C and Yuan Yang A D
+ Author Affiliations
- Author Affiliations

A Department of Medical Genetics, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, Sichuan, 610041, China.

B Jinjiang Maternal and Child Health Hospital, Chengdu, Sichuan, 610011, China.

C Reproductive Medicine Institute, Chengdu Women’s and Children’s Central Hospital, Chengdu, Sichuan, 610031, China.

D Corresponding author. Email: yangyuan@scu.edu.cn

Reproduction, Fertility and Development 30(3) 555-562 https://doi.org/10.1071/RD17146
Submitted: 13 April 2017  Accepted: 5 August 2017   Published: 29 August 2017

Abstract

Testis-specific protein, Y-encoded, 1 (TSPY1) is involved in the regulation of spermatogenic efficiency via highly variable copy dosage, with dosage deficiency of the multicopy gene conferring an increased risk of spermatogenic failure. TSPY-like 1 (TSPYL1) and TSPY-like 5 (TSPYL5), two autosomal homologous genes originating from TSPY1, share a core sequence that encodes a functional nucleosome assembly protein (NAP) domain with TSPY1. To explore the potential effects of TSPYL1 and TSPYL5 on the TSPY1-related spermatogenic phenotype, we investigated the expression of these genes in 15 healthy and nonpathological human tissues (brain, kidney, liver, pancreas, thymus, prostate, spleen, muscle, leucocytes, placenta, intestine, ovary, lung, colon and testis) and explored associations between their variations and spermatogenic failure in 1558 Han Chinese men with different spermatogenic conditions, including 304 men with TSPY1 dosage deficiency. TSPYL1 and TSPYL5 were expressed in many different tissues, including the testis. An unreported rare variant that is likely pathogenic (c.1057A>G, p.Thr353Ala) and another of uncertain significance (c.1258C>T, p.Arg420Cys) in the NAP-coding sequence of TSPYL1 were observed in three spermatogenesis-impaired patients with heterozygous status. The distribution differences in the alleles, genotypes and haplotypes of eight TSPYL1- and TSPYL5-linked common variants did not reach statistical significance in comparisons of patients with spermatogenic failure and controls with normozoospermia. No difference in sperm production was observed among men with different genotypes of the variants. Similar results were obtained in men with TSPY1 dosage deficiencies. Although the distribution of missense variants of TSPYL1 found in the present and other studies suggests that patients with spermatogenic failure may have a statistically significant greater burden of rare variations in TSPYL1 relative to normozoospermic controls, the functional evidence suggests that TSPYL1 contributes to impaired spermatogenesis. Moreover, the present study suggests that the effects of TSPYL1 and TSPYL5 on the spermatogenic phenotype of TSPY1 dosage deficiency are limited, which may be due to the stability of their function resulting from high sequence conservation.

Additional keywords: autosomal homologous genes, gene family, male infertility, single nucleotide polymorphisms, sperm production, spermatogenesis, variation, Y chromosome-linked gene.


References

Åberg, K., Adkins, D. E., Liu, Y., McClay, J. L., Bukszár, J., Jia, P., Zhao, Z., Perkins, D., Stroup, T. S., Lieberman, J. A., Sullivan, P. F., and van den Oord, E. J. C. G. (2012). Genome-wide association study of antipsychotic-induced QTc interval prolongation. Pharmacogenomics J. 12, 165–172.
Genome-wide association study of antipsychotic-induced QTc interval prolongation.Crossref | GoogleScholarGoogle Scholar |

Anttila, V., Stefansson, H., Kallela, M., Todt, U., Terwindt, G. M., Calafato, M. S., Nyholt, D. R., Dimas, A. S., Freilinger, T., Müller-Myhsok, B., Artto, V., Inouye, M., Alakurtti, K., Kaunisto, M. A., Hämäläinen, E., de Vries, B., Stam, A. H., Weller, C. M., Heinze, A., Heinze-Kuhn, K., Goebel, I., Borck, G., Göbel, H., Steinberg, S., Wolf, C., Björnsson, A., Gudmundsson, G., Kirchmann, M., Hauge, A., Werge, T., Schoenen, J., Eriksson, J. G., Hagen, K., Stovner, L., Wichmann, H. E., Meitinger, T., Alexander, M., Moebus, S., Schreiber, S., Aulchenko, Y. S., Breteler, M. M., Uitterlinden, A. G., Hofman, A., van Duijn, C. M., Tikka-Kleemola, P., Vepsäläinen, S., Lucae, S., Tozzi, F., Muglia, P., Barrett, J., Kaprio, J., Färkkilä, M., Peltonen, L., Stefansson, K., Zwart, J. A., Ferrari, M. D., Olesen, J., Daly, M., Wessman, M., van den Maagdenberg, A. M., Dichgans, M., Kubisch, C., Dermitzakis, E. T., Frants, R. R., Palotie, A., International Headache Genetics Consortium (2010). Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat. Genet. 42, 869–873.
Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyiu73P&md5=56276fd59f3cccff1e0ee90858af5735CAS |

Bellott, D. W., Hughes, J. F., Skaletsky, H., Brown, L. G., Pyntikova, T., Cho, T. J., Koutseva, N., Zaghlul, S., Graves, T., Rock, S., Kremitzki, C., Fulton, R. S., Dugan, S., Ding, Y., Morton, D., Khan, Z., Lewis, L., Buhay, C., Wang, Q., Watt, J., Holder, M., Lee, S., Nazareth, L., Alföldi, J., Rozen, S., Muzny, D. M., Warren, W. C., Gibbs, R. A., Wilson, R. K., and Page, D. C. (2014). Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508, 494–499.
Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmslaktbg%3D&md5=c664cfcfc8b55db45a662683c7f2006dCAS |

Chen, D., Zheng, W., Lin, A., Uyhazi, K., Zhao, H., and Lin, H. (2012). Pumilio 1 suppresses multiple activators of p53 to safeguard spermatogenesis. Curr. Biol. 22, 420–425.
Pumilio 1 suppresses multiple activators of p53 to safeguard spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisFKmsrg%3D&md5=27ae5711b162c555bd2270e50ac4c037CAS |

Cooper, T. G., Noonan, E., von Eckardstein, S., Auger, J., Baker, H. W., Behre, H. M., Haugen, T. B., Kruger, T., Wang, C., Mbizvo, M. T., and Vogelsong, K. M. (2010). World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 16, 231–245.
World Health Organization reference values for human semen characteristics.Crossref | GoogleScholarGoogle Scholar |

Epping, M. T., Meijer, L. A., Krijgsman, O., Bos, J. L., Pandolfi, P. P., and Bernards, R. (2011). TSPYL5 suppresses p53 levels and function by physical interaction with USP7. Nat. Cell Biol. 13, 102–108.
TSPYL5 suppresses p53 levels and function by physical interaction with USP7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyksr%2FJ&md5=2ad83ec1689053f7fa8bf3022d690a5aCAS |

Ertiro, B. T., Ogugo, V., Worku, M., Das, B., Olsen, M., Labuschagne, M., and Semagn, K. (2015). Comparison of Kompetitive Allele Specific PCR (KASP) and genotyping by sequencing (GBS) for quality control analysis in maize. BMC Genomics 16, 908.
Comparison of Kompetitive Allele Specific PCR (KASP) and genotyping by sequencing (GBS) for quality control analysis in maize.Crossref | GoogleScholarGoogle Scholar |

Giachini, C., Nuti, F., Turner, D. J., Laface, I., Xue, Y., Daguin, F., Forti, G., Tyler-Smith, C., and Krausz, C. (2009). TSPY1 copy number variation influences spermatogenesis and shows differences among Y lineages. J. Clin. Endocrinol. Metab. 94, 4016–4022.
TSPY1 copy number variation influences spermatogenesis and shows differences among Y lineages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12ru7fI&md5=496265e31c20a3ac5290c1d4f322717aCAS |

He, C., Holme, J., and Anthony, J. (2014). SNP genotyping: the KASP assay. Methods Mol. Biol. 1145, 75–86.
SNP genotyping: the KASP assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnvVWntLg%3D&md5=4fdf9574722c0ff2df5ac66c91034db1CAS |

Javaher, P., Stuhrmann, M., Wilke, C., Frenzel, E., Manukjan, G., Grosshenig, A., Dechend, F., Schwaab, E., Schmidtke, J., and Schubert, S. (2012). Should TSPYL1 mutation screening be included in routine diagnostics of male idiopathic infertility? Fertil. Steril. 97, 402–406.
Should TSPYL1 mutation screening be included in routine diagnostics of male idiopathic infertility?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVeru7g%3D&md5=0b9ee7dc8164e065b6efdb76135f9286CAS |

Kellogg, D. R., Kikuchi, A., Fujii-Nakata, T., Turck, C. W., and Murray, A. W. (1995). Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J. Cell Biol. 130, 661–673.
Members of the NAP/SET family of proteins interact specifically with B-type cyclins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntFWhtbc%3D&md5=afe39a472c5b0969644c09d421b8a41bCAS |

Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U., and Segal, E. (2007). The role of site accessibility in microRNA target recognition. Nat. Genet. 39, 1278–1284.
The role of site accessibility in microRNA target recognition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtV2isL7P&md5=e4e56ae86156b6a1719cf3408bd4742eCAS |

Kim, E. J., Lee, S. Y., Kim, T. R., Choi, S. I., Cho, E. W., Kim, K. C., and Kim, I. G. (2010). TSPYL5 is involved in cell growth and the resistance to radiation in A549 cells via the regulation of p21(WAF1/Cip1) and PTEN/AKT pathway. Biochem. Biophys. Res. Commun. 392, 448–453.
TSPYL5 is involved in cell growth and the resistance to radiation in A549 cells via the regulation of p21(WAF1/Cip1) and PTEN/AKT pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVKjsrw%3D&md5=e3fce0280d197e1e058148da736c6399CAS |

Krausz, C., Hoefsloot, L., Simoni, M., Tüttelmann, F., European Academy of Andrology and European Molecular Genetics Quality Network (2014). EAA/EMQN best practice guidelines for molecular diagnosis of Y-chromosomal microdeletions: state-of-the-art 2013. Andrology 2, 5–19.
EAA/EMQN best practice guidelines for molecular diagnosis of Y-chromosomal microdeletions: state-of-the-art 2013.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVSqtL7F&md5=9d111e5ab1069c0a961261250faebf97CAS |

Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., and Rajewsky, N. (2005). Combinatorial microRNA target predictions. Nat. Genet. 37, 495–500.
Combinatorial microRNA target predictions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsF2ksrw%3D&md5=4be62adfdd4e3f9edfd5b930d1d52ea4CAS |

Krude, T. (1999). Chromatin assembly during DNA replication in somatic cells. Eur. J. Biochem. 263, 1–5.
Chromatin assembly during DNA replication in somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslKrs7k%3D&md5=8dfabea35514ea516c659be5eed360a2CAS |

Kwong, A. K., Fung, C. W., Chan, S. Y., and Wong, V. C. (2012). Identification of SCN1A and PCDH19 mutations in Chinese children with Dravet syndrome. PLoS One 7, e41802.
Identification of SCN1A and PCDH19 mutations in Chinese children with Dravet syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFanu7rJ&md5=5d68064e12d71e367ef92c3ce1b39a64CAS |

Lau, Y. F., Li, Y., and Kido, T. (2009). Gonadoblastoma locus and the TSPY gene on the human Y chromosome. Birth Defects Res. C Embryo Today 87, 114–122.
Gonadoblastoma locus and the TSPY gene on the human Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKrs7s%3D&md5=76da951b4eb5ca70c32833a84b2ee3acCAS |

Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20.
Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXot1ChsA%3D%3D&md5=4b020df4a2b6450b3dc29b75fedcd451CAS |

Liang, Y., Zhang, R., Zhang, S., Ji, G., Shi, P., Yang, T., Liu, F., Feng, J., Li, C., Guo, D., and Chen, M. (2016). Association of ACYP2 and TSPYL6 genetic polymorphisms with risk of ischemic stroke in Han Chinese population. Mol. Neurobiol. , .
Association of ACYP2 and TSPYL6 genetic polymorphisms with risk of ischemic stroke in Han Chinese population.Crossref | GoogleScholarGoogle Scholar |

Liu, M., Li, B., Guo, W., Zhang, X., Chen, Z., Li, J., Yan, M., Chen, C., and Jin, T. (2016). Association between single nucleotide polymorphisms in the TSPYL6 gene and breast cancer susceptibility in the Han Chinese population. Oncotarget 7, 54771–54781.
Association between single nucleotide polymorphisms in the TSPYL6 gene and breast cancer susceptibility in the Han Chinese population.Crossref | GoogleScholarGoogle Scholar |

Liu, M., Ingle, J. N., Fridley, B. L., Buzdar, A. U., Robson, M. E., Kubo, M., Wang, L., Batzler, A., Jenkins, G. D., Pietrzak, T. L., Carlson, E. E., Goetz, M. P., Northfelt, D. W., Perez, E. A., Williard, C. V., Schaid, D. J., Nakamura, Y., and Weinshilboum, R. M. (2013). TSPYL5 SNPs: association with plasma estradiol concentrations and aromatase expression. Mol. Endocrinol. 27, 657–670.
TSPYL5 SNPs: association with plasma estradiol concentrations and aromatase expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVant7o%3D&md5=c3a1ef65585a73875013fae8f1110cc6CAS |

McQuibban, G. A., Commisso-Cappelli, C. N., and Lewis, P. N. (1998). Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1. J. Biol. Chem. 273, 6582–6590.
Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFaltb0%3D&md5=ca1e0e971cb7d15840251fac35c769d4CAS |

Neto, F. T., Bach, P. V., Najari, B. B., Li, P. S., and Goldstein, M. (2016). Spermatogenesis in humans and its affecting factors. Semin. Cell Dev. Biol. 59, 10–26.
Spermatogenesis in humans and its affecting factors.Crossref | GoogleScholarGoogle Scholar |

Norling, A., Hirschberg, A. L., Rodriguez-Wallberg, K. A., Iwarsson, E., Wedell, A., and Barbaro, M. (2014). Identification of a duplication within the GDF9 gene and novel candidate genes for primary ovarian insufficiency (POI) by a customized high-resolution array comparative genomic hybridization platform. Hum. Reprod. 29, 1818–1827.
Identification of a duplication within the GDF9 gene and novel candidate genes for primary ovarian insufficiency (POI) by a customized high-resolution array comparative genomic hybridization platform.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1SqtrjF&md5=11bdfe01c010475470b04ad1ab2606b1CAS |

Puffenberger, E. G., Hu-Lince, D., Parod, J. M., Craig, D. W., Dobrin, S. E., Conway, A. R., Donarum, E. A., Strauss, K. A., Dunckley, T., Cardenas, J. F., Melmed, K. R., Wright, C. A., Liang, W., Stafford, P., Flynn, C. R., Morton, D. H., and Stephan, D. A. (2004). Mapping of sudden infant death with dysgenesis of the testes syndrome (SIDDT) by a SNP genome scan and identification of TSPYL loss of function. Proc. Natl. Acad. Sci. USA 101, 11689–11694.
Mapping of sudden infant death with dysgenesis of the testes syndrome (SIDDT) by a SNP genome scan and identification of TSPYL loss of function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntVeku70%3D&md5=105b7dabd37a8af698c5fbca6c9d5cfcCAS |

Rentería, M. E., Coolen, M. W., Statham, A. L., Choi, R. S., Qu, W., Campbell, M. J., Smith, S., Henders, A. K., Montgomery, G. W., Clark, S. J., Martin, N. G., and Medland, S. E. (2013). GWAS of DNA methylation variation within imprinting control regions suggests parent-of-origin association. Twin Res. Hum. Genet. 16, 767–781.
GWAS of DNA methylation variation within imprinting control regions suggests parent-of-origin association.Crossref | GoogleScholarGoogle Scholar |

Richards, S., Aziz, N., Bale, S., Bick, D., Das, S., Gastier-Foster, J., Grody, W. W., Hegde, M., Lyon, E., Spector, E., Voelkerding, K., Rehm, H. L., ACMG Laboratory Quality Assurance Committee (2015). Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet. Med. 17, 405–423.
Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology.Crossref | GoogleScholarGoogle Scholar |

Schnieders, F., Dörk, T., Arnemann, J., Vogel, T., Werner, M., and Schmidtke, J. (1996). Testis-specific protein, Y-encoded (TSPY) expression in testicular tissues. Hum. Mol. Genet. 5, 1801–1807.
Testis-specific protein, Y-encoded (TSPY) expression in testicular tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslKlsrs%3D&md5=8b9f67f9eaec44d2fc22a2e05af7482dCAS |

Shen, Y., Yan, Y., Liu, Y., Zhang, S., Yang, D., Zhang, P., Li, L., Wang, Y., Ma, Y., Tao, D., and Yang, Y. (2013). A significant effect of the TSPY1 copy number on spermatogenesis efficiency and the phenotypic expression of the gr/gr deletion. Hum. Mol. Genet. 22, 1679–1695.
A significant effect of the TSPY1 copy number on spermatogenesis efficiency and the phenotypic expression of the gr/gr deletion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWhsro%3D&md5=2a3dc755507a12d57b8be7dba888f248CAS |

Shi, Y. Y., and He, L. (2005). SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res. 15, 97–98.
SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFynsro%3D&md5=5b428a3a31220399832ab3d6ec2ce002CAS |

Shikama, N., Chan, H. M., Krstic-Demonacos, M., Smith, L., Lee, C. W., Cairns, W., and La Thangue, N. B. (2000). Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators. Mol. Cell. Biol. 20, 8933–8943.
Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFGrs7o%3D&md5=1e37d40cb336e72f6cd470fa2c995f2aCAS |

Skaletsky, H., Kuroda-Kawaguchi, T., Minx, P. J., Cordum, H. S., Hillier, L., Brown, L. G., Repping, S., Pyntikova, T., Ali, J., Bieri, T., Chinwalla, A., Delehaunty, A., Delehaunty, K., Du, H., Fewell, G., Fulton, L., Fulton, R., Graves, T., Hou, S. F., Latrielle, P., Leonard, S., Mardis, E., Maupin, R., McPherson, J., Miner, T., Nash, W., Nguyen, C., Ozersky, P., Pepin, K., Rock, S., Rohlfing, T., Scott, K., Schultz, B., Strong, C., Tin-Wollam, A., Yang, S. P., Waterston, R. H., Wilson, R. K., Rozen, S., and Page, D. C. (2003). The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837.
The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1Kmtbk%3D&md5=81e76d03a455b19e099280405f22cbcfCAS |

Vinci, G., Brauner, R., Tar, A., Rouba, H., Sheth, J., Sheth, F., Ravel, C., McElreavey, K., and Bashamboo, A. (2009). Mutations in the TSPYL1 gene associated with 46,XY disorder of sex development and male infertility. Fertil. Steril. 92, 1347–1350.
Mutations in the TSPYL1 gene associated with 46,XY disorder of sex development and male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaisbrF&md5=522cb8cbec3430e72f3ca3d1ceb22627CAS |

Vogel, T., Dittrich, O., Mehraein, Y., Dechend, F., Schnieders, F., and Schmidtke, J. (1998). Murine and human TSPYL genes: novel members of the TSPY-SET-NAP1L1 family. Cytogenet. Cell Genet. 81, 265–270.
Murine and human TSPYL genes: novel members of the TSPY-SET-NAP1L1 family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtlOrtL4%3D&md5=71856e48067e4939cfe59a93eaa9d94bCAS |

Wilhelm, D., Palmer, S., and Koopman, P. (2007). Sex determination and gonadal development in mammals. Physiol. Rev. 87, 1–28.
Sex determination and gonadal development in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVahu7o%3D&md5=ea01c383f48fdb7be1cfe423302fc3b2CAS |

Yang, Q., Hua, J., Wang, L., Xu, B., Zhang, H., Ye, N., Zhang, Z., Yu, D., Howard, J., Zhang, Y., and Shi, Q. (2013). MicroRNA and piRNA profiles in normal human testis detected by nextgeneration sequencing. PLoS One 8, e66809.
MicroRNA and piRNA profiles in normal human testis detected by nextgeneration sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVyht7vL&md5=bcf776ba526393b02cc77ae1d73f1c3bCAS |

Yin, Y. H., Li, Y. Y., Qiao, H., Wang, H. C., Yang, X. A., Zhang, H. G., Pang, X. W., Zhang, Y., and Chen, W. F. (2005). TSPY is a cancer testis antigen expressed in human hepatocellular carcinoma. Br. J. Cancer 93, 458–463.
TSPY is a cancer testis antigen expressed in human hepatocellular carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnvFymtbY%3D&md5=7a7faca7eacd360cdd7473a6f471247aCAS |