An integrated analysis of second- and third-generation transcriptome sequencing technologies reveals the DAZAP1 function in pig testis
Xia Zhang; Hailong Huo; Honglin Li; Yongqing Liu; Fujie Qiao; Changyao Li; Jinlong Huo
Abstract
Keywords
References
Abramson J, Adler J, Dunger J, Evans R, Green T, Pritzel A, Ronneberger O, Willmore L, Ballard AJ, Bambrick J, Bodenstein SW, Evans DA, Hung CC, O’Neill M, Reiman D, Tunyasuvunakool K, Wu Z, Žemgulytė A, Arvaniti E, Beattie C, Bertolli O, Bridgland A, Cherepanov A, Congreve M, Cowen-Rivers AI, Cowie A, Figurnov M, Fuchs FB, Gladman H, Jain R, Khan YA, Low CMR, Perlin K, Potapenko A, Savy P, Singh S, Stecula A, Thillaisundaram A, Tong C, Yakneen S, Zhong ED, Zielinski M, Žídek A, Bapst V, Kohli P, Jaderberg M, Hassabis D, Jumper JM. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature. 2024;630(8016):493-500.
Blencowe BJ. Alternative splicing: new insights from global analyses. Cell. 2006;126(1):37-47.
Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 2004;4(6):1633-49.
Cai Y, Yu X, Hu S, Yu J. A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics. 2009;7(4):147-54.
Chen L, Lin X, Lei Y, Xu X, Zhou Q, Chen Y, Liu H, Jiang J, Yang Y, Zheng F, Wu B. Aerobic glycolysis enhances HBx-initiated hepatocellular carcinogenesis via NF-κBp65/HK2 signalling. J Exp Clin Cancer Res. 2022;41(1):329.
Chen YT, Iseli C, Venditti CA, Old LJ, Simpson AJ, Jongeneel CV. Identification of a new cancer/testis gene family, CT47, among expressed multicopy genes on the human X chromosome. Genes Chromosomes Cancer. 2006;45(4):392-400.
Cheng CY, Mruk DD. The biology of spermatogenesis: the past, present and future. Philos Trans R Soc Lond B Biol Sci. 2010;365(1546):1459-63.
Cheng LJ, Li JM, Chen J, Ge YH, Yu ZR, Han DS, Zhou ZM, Sha JH. NYD-SP16, a novel gene associated with spermatogenesis of human testis. Biol Reprod. 2003;68(1):190-8.
Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB, Eddy EM. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet. 2001;28(1):82-6.
Dai T, Vera Y, Salido EC, Yen PH. Characterization of the mouse Dazap1 gene encoding an RNA-binding protein that interacts with infertility factors DAZ and DAZL. BMC Genomics. 2001;2(1):6.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15-21.
Gao Y, Wang Y, Chen X, Peng Y, Chen F, He Y, Pang W, Yang G, Yu T. MiR-127 attenuates adipogenesis by targeting MAPK4 and HOXC6 in porcine adipocytes. J Cell Physiol. 2019;234(12):21838-50.
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the expasy server. In: John M. Walker: The Proteomics Protocols Handbook, Humana Press, 2005. pp. 571-607.
Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N. Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil. 2015;16(2):61-71. PMid:25927022.
Hao F, Kale S, Dimitrov S, Hayes JJ. Unraveling linker histone interactions in nucleosomes. Curr Opin Struct Biol. 2021;71:87-93.
Hao F, Murphy KJ, Kujirai T, Kamo N, Kato J, Koyama M, Okamato A, Hayashi G, Kurumizaka H, Hayes JJ. Acetylation-modulated communication between the H3 N-terminal tail domain and the intrinsically disordered H1 C-terminal domain. Nucleic Acids Res. 2020;48(20):11510-20.
Hsu LC, Chen HY, Lin YW, Chu WC, Lin MJ, Yan YT, Yen PH. DAZAP1, an hnRNP protein, is required for normal growth and spermatogenesis in mice. RNA. 2008;14(9):1814-22.
Hu T, Chitnis N, Monos D, Dinh A. Next-generation sequencing technologies: an overview. Hum Immunol. 2021;82(11):801-11.
Huo JL, Zhang LQ, Zhang X, Wu XW, Ye XH, Sun YH, Cheng WM, Yang K, Pan WR, Zeng YZ. Genome-wide single nucleotide polymorphism array and whole-genome sequencing reveal the inbreeding progression of Banna minipig inbred line. Anim Genet. 2022;53(1):146-51.
Ito C, Makino T, Mutoh T, Kikkawa M, Toshimori K. The association of ODF4 with AK1 and AK2 in mice is essential for fertility through its contribution to flagellar shape. Sci Rep. 2023;13(1):2969.
Kim YH, Han ME, Oh SO. The molecular mechanism for nuclear transport and its application. Anat Cell Biol. 2017;50(2):77-85.
Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat. 1952;90(2):167-215.
Lee Y, Rio DC. Mechanisms and regulation of alternative Pre-mRNA splicing. Annu Rev Biochem. 2015;84(1):291-323.
Lin YT, Yen PH. A novel nucleocytoplasmic shuttling sequence of DAZAP1, a testis-abundant RNA-binding protein. RNA. 2006;12(8):1486-93.
Manjunath P, Bergeron A, Lefebvre J, Fan J. Seminal plasma proteins: functions and interaction with protective agents during semen preservation. Soc Reprod Fertil Suppl. 2007;65:217-28. PMid:17644964.
Morton S, Yang HT, Moleleki N, Campbell DG, Cohen P, Rousseau S. Phosphorylation of the ARE-binding protein DAZAP1 by ERK2 induces its dissociation from DAZ. Biochem J. 2006;399(2):265-73.
Neilson LI, Schneider PA, Van Deerlin PG, Kiriakidou M, Driscoll DA, Pellegrini MC, Millinder S, Yamamoto KK, French CK, Strauss JF 3rd. cDNA cloning and characterization of a human sperm antigen (SPAG6) with homology to the product of the Chlamydomonas PF16 locus. Genomics. 1999;60(3):272-80.
Neto FT, Bach PV, Najari BB, Li PS, Goldstein M. Spermatogenesis in humans and its affecting factors. Semin Cell Dev Biol. 2016;59:10-26.
Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010;465(7301):1033-8.
Rao X, Huang X, Zhou Z, Lin X. An improvement of the 2^(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat Bioinforma Biomath. 2013;3(3):71-85. PMid:25558171.
Reijo R, Lee TY, Salo P, Alagappan R, Brown LG, Rosenberg M, Rozen S, Jaffe T, Straus D, Hovatta O, de la Chapelle A, Silber S, Page DC. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat Genet. 1995;10(4):383-93.
Reijo RA, Dorfman DM, Slee R, Renshaw AA, Loughlin KR, Cooke H, Page DC. DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol Reprod. 2000;63(5):1490-6.
Rha J, Jones SK, Fidler J, Banerjee A, Leung SW, Morris KJ, Wong JC, Inglis GAS, Shapiro L, Deng Q, Cutler AA, Hanif AM, Pardue MT, Schaffer A, Seyfried NT, Moberg KH, Bassell GJ, Escayg A, García PS, Corbett AH. The RNA-binding protein, ZC3H14, is required for proper poly(A) tail length control, expression of synaptic proteins, and brain function in mice. Hum Mol Genet. 2017;26(19):3663-81.
Sahoo B, Choudhary RK, Sharma P, Choudhary S, Gupta MK. Significance and Relevance of Spermatozoal RNAs to Male Fertility in Livestock. Front Genet. 2021;12:768196.
Sapay N, Guermeur Y, Deléage G. Prediction of amphipathic in-plane membrane anchors in monotopic proteins using a SVM classifier. BMC Bioinformatics. 2006;7(1):255.
Sasaki K, Ono M, Takabe K, Suzuki A, Kurihara Y. Specific intron-dependent loading of DAZAP1 onto the cox6c transcript suppresses pre-mRNA splicing efficacy and induces cell growth retardation. Gene. 2018;657:1-8.
Saxena R, Brown LG, Hawkins T, Alagappan RK, Skaletsky H, Reeve MP, Reijo R, Rozen S, Dinulos MB, Disteche CM, Page DC. The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat Genet. 1996;14(3):292-9.
Smith RW, Anderson RC, Smith JW, Brook M, Richardson WA, Gray NK. DAZAP1, an RNA-binding protein required for development and spermatogenesis, can regulate mRNA translation. RNA. 2011;17(7):1282-95.
Tsui S, Dai T, Roettger S, Schempp W, Salido EC, Yen PH. Identification of two novel proteins that interact with germ-cell-specific RNA-binding proteins DAZ and DAZL1. Genomics. 2000;65(3):266-73.
Vera Y, Dai T, Hikim AP, Lue Y, Salido EC, Swerdloff RS, Yen PH. Deleted in azoospermia associated protein 1 shuttles between nucleus and cytoplasm during normal germ cell maturation. J Androl. 2002;23(5):622-8.
Wang P, Zhang X, Huo H, Li W, Liu Z, Wang L, Li L, Sun YH, Huo J. Transcriptomic analysis of testis and epididymis tissues from Banna mini-pig inbred line boars with single-molecule long-read sequencing. Biol Reprod. 2023;108(3):465-78.
Wang Q, Guo Y, Wang W, Liu B, Yang G, Xu Z, Li J, Liu Z. RNA binding protein DAZAP1 promotes HCC progression and regulates ferroptosis by interacting with SLC7A11 mRNA. Exp Cell Res. 2021;399(1):112453.
Wu H, Wang J, Cheng H, Gao Y, Liu W, Zhang Z, Jiang H, Li W, Zhu F, Lv M, Liu C, Tan Q, Zhang X, Wang C, Ni X, Chen Y, Song B, Zhou P, Wei Z, Zhang F, He X, Cao Y. Patients with severe asthenoteratospermia carrying SPAG6 or RSPH3 mutations have a positive pregnancy outcome following intracytoplasmic sperm injection. J Assist Reprod Genet. 2020;37(4):829-40.
Xie Y, Cao H, Zhang Z, Zhang S, Wang H. Molecular network of miR-1343 regulates the pluripotency of porcine pluripotent stem cells via repressing OTX2 expression. RNA Biol. 2019;16(1):82-92.
Yan Q, Wu X, Chen C, Diao R, Lai Y, Huang J, Chen J, Yu Z, Gui Y, Tang A, Cai Z. Developmental expression and function of DKKL1/Dkkl1 in humans and mice. Reprod Biol Endocrinol. 2012;10(1):51.
Yang HT, Peggie M, Cohen P, Rousseau S. DAZAP1 interacts via its RNA-recognition motifs with the C-termini of other RNA-binding proteins. Biochem Biophys Res Commun. 2009;380(3):705-9.
You X, Chen Q, Yuan D, Zhang C, Zhao H. Common markers of testicular Sertoli cells. Expert Rev Mol Diagn. 2021;21(6):613-26.
Submitted date:
12/31/2024
Accepted date:
05/09/2025