Genes & Genomics

, Volume 40, Issue 7, pp 781–787 | Cite as

LncRNA Gm2044 highly expresses in spermatocyte and inhibits Utf1 translation by interacting with Utf1 mRNA

  • Ke Hu
  • Leina Li
  • Yaping Liao
  • Meng Liang
Research Article


Spermatogenesis is a process which includes the following phases: spermatogonial stem cell proliferation and differentiation, spermatogonia, spermatocyte, spermatid and mature sperm. Spermatogenic failure is the important factor resulting in male infertility. Recent studies showed that long noncoding RNA (lncRNA) have been found to be involved in the regulation of male reproduction. However, lncRNA associated with spermatogenesis and their mechanisms of action are unclear. The aim of this study is to explore the role and molecular mechanism of lncRNA in spermatogenesis. LncRNA microarray of germ cells and bioinformatic analysis showed lncRNA Gm2044 may play potential roles in spermatogenesis. The expression level of RNA and protein were analyzed by RT-qPCR and western blotting, respectively. The interaction of lncRNA with mRNA was detected by RNA pull down and cellular proliferation was measured using CCK-8 reagent. Testis-enriched lncRNA Gm2044 is abundant in mouse spermatocytes. Gm2044 can suppress the translation of adjacent spermatogenesis-related gene Utf1 by interacting with Utf1 mRNA. Furthermore, the proliferation of mouse spermatogonia GC-1 cell line and spermatocyte GC-2 cell line was inhibited by Gm2044. CONCLUSION: LncRNA Gm2044 was identified to inhibit Utf1 mRNA translation and play important roles in spermatogenesis.


LncRNA Gm2044 Spermatocyte UTF1 GC-1 GC-2 



This work was supported by Natural Science Foundation of Anhui Province (China) (1608085QH199), Natural Science Foundation of Bengbu Medical College (China) (BYKY1406ZD), Undergraduate Training Program for Innovation and Entrepreneurship of Anhui Province (China) (201610367003) and Research Foundation for Excellent Youth Scholars of Anhui Provincial Department of Education (China) (2012SQRL092). We thank Dr. Fei Sun (Shanghai Jiaotong University, China) for offering GC-1 and GC-2 cell lines.

Author contributions

KH and ML conceived and performed this research; ML wrote this manuscript, LL and YL analyzed results and reviewed this manuscript.

Compliance with ethical standards

Conflict of interest

Ke Hu declares that she has no conflict of interest. Leina Li declares that she has no conflict of interest. Yaping Liao declares that he has no conflict of interest. Meng Liang declares that he has no conflict of interest.

Ethical approval

This study received ethical approval from the institutional review boards of the Bengbu medical college.

Supplementary material

13258_2018_690_MOESM1_ESM.docx (133 kb)
Supplementary material 1 (DOCX 133 KB)


  1. Agbor VA, Tao S, Lei N, Heckert LL (2013) A Wt1-Dmrt1 transgene restores DMRT1 to sertoli cells of Dmrt1(−/−) testes: a novel model of DMRT1-deficient germ cells. Biol Reprod 88:51CrossRefPubMedGoogle Scholar
  2. Akhade VS, Dighe SN, Kataruka S, Rao MR (2016) Mechanism of Wnt signaling induced down regulation of mrhl long non-coding RNA in mouse spermatogonial cells. Nucleic Acids Res 44:387–401CrossRefPubMedGoogle Scholar
  3. Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ 3rd, Lee JT (2011) Tsx produces a long noncoding RNA and has general functions in the germline, stem cells, and brain. PLoS Genet 7:e1002248CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arun G, Akhade VS, Donakonda S, Rao MR (2012) mrhl RNA, a long noncoding RNA, negatively regulates Wnt signaling through its protein partner Ddx5/p68 in mouse spermatogonial cells. Mol Cell Biol 32:3140–3152CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ayoub N, Richler C, Wahrman J (1997) Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis. Chromosoma 106:1–10CrossRefPubMedGoogle Scholar
  6. Bao J, Wu J, Schuster AS, Hennig GW, Yan W (2013) Expression profiling reveals developmentally regulated lncRNA repertoire in the mouse male germline. Biol Reprod 89:107CrossRefPubMedPubMedCentralGoogle Scholar
  7. de Rooij DG, Russell LD (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21:776–798PubMedGoogle Scholar
  8. Easley CA, Phillips BT, McGuire MM, Barringer JM, Valli H, Hermann BP, Simerly CR, Rajkovic A, Miki T, Orwig KE, Schatten GP (2012) Direct differentiation of human pluripotent stem cells into haploid spermatogenic cells. Cell Rep 2:440–446CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hu K, Zhang J, Liang M (2017) LncRNA AK015322 promotes proliferation of spermatogonial stem cell C18-4 by acting as a decoy for microRNA-19b-3p. In Vitro Cell Dev 53(3):277–284CrossRefGoogle Scholar
  10. Jung H, Roser JF, Yoon M (2014) UTF1, a putative marker for spermatogonial stem cells in stallions. PLoS ONE 9:e108825CrossRefPubMedPubMedCentralGoogle Scholar
  11. Keene JD (2007) Biological clocks and the coordination theory of RNA operons and regulons. Cold Spring Harb Sym 72:157–165CrossRefGoogle Scholar
  12. Lee TL, Xiao A, Rennert OM (2012) Identification of novel long noncoding RNA transcripts in male germ cells. Methods Mol Biol 825:105–114CrossRefPubMedPubMedCentralGoogle Scholar
  13. Li L, Wang M, Wu X, Geng L, Xue Y, Wei X, Jia Y (2016) A long non-coding RNA interacts with Gfra1 and maintains survival of mouse spermatogonial stem cells. Cell Death Dis 7:e2140CrossRefPubMedPubMedCentralGoogle Scholar
  14. Liang M, Li W, Tian H, Hu T, Wang L, Lin Y, Li Y, Huang H, Sun F (2014) Sequential expression of long noncoding RNA as mRNA gene expression in specific stages of mouse spermatogenesis. Sci Rep 4:5966CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lu M, Tian H, Cao YX, He X, Chen L, Song X, Ping P, Huang H, Sun F (2015) Downregulation of miR-320a/383-sponge-like long non-coding RNA NLC1-C (narcolepsy candidate-region 1 genes) is associated with male infertility and promotes testicular embryonal carcinoma cell proliferation. Cell Death Dis 6:e1960CrossRefPubMedPubMedCentralGoogle Scholar
  16. Luk AC, Chan WY, Rennert OM, Lee TL (2014) Long noncoding RNAs in spermatogenesis: insights from recent high-throughput transcriptome studies. Reproduction 147:R131–R141CrossRefPubMedGoogle Scholar
  17. Raverdeau M, Gely-Pernot A, Feret B, Dennefeld C, Benoit G, Davidson I, Chambon P, Mark M, Ghyselinck NB (2012) Retinoic acid induces sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis. Proc Natl Acad Sci USA 109:16582–16587CrossRefPubMedPubMedCentralGoogle Scholar
  18. Salido EC, Yen PH, Mohandas TK, Shapiro LJ (1992) Expression of the X-inactivation-associated gene XIST during spermatogenesis. Nat Genet 2:196–199CrossRefPubMedGoogle Scholar
  19. Sun J, Wu J (2015) Expression profiling of long noncoding RNAs in neonatal and adult mouse testis. Data Brief 4:322–327CrossRefPubMedPubMedCentralGoogle Scholar
  20. Sun J, Lin Y, Wu J (2013) Long non-coding RNA expression profiling of mouse testis during postnatal development. PLoS ONE 8:e75750CrossRefPubMedPubMedCentralGoogle Scholar
  21. van Bragt MP, Roepers-Gajadien HL, Korver CM, Bogerd J, Okuda A, Eggen BJ, de Rooij DG, van Pelt AM (2008) Expression of the pluripotency marker UTF1 is restricted to a subpopulation of early A spermatogonia in rat testis. Reproduction 136:33–40CrossRefPubMedGoogle Scholar
  22. Wen K, Yang L, Xiong T, Di C, Ma D, Wu M, Xue Z, Zhang X, Long L, Zhang W, Zhang J, Bi X, Dai J, Zhang Q, Lu ZJ, Gao G (2016) Critical roles of long noncoding RNAs in Drosophila spermatogenesis. Genome Res 26:1233–1244CrossRefPubMedPubMedCentralGoogle Scholar
  23. Yoneda R, Satoh Y, Yoshida I, Kawamura S, Kotani T, Kimura AP (2016) A genomic region transcribed into a long noncoding RNA interacts with the Prss42/Tessp-2 promoter in spermatocytes during mouse spermatogenesis, and its flanking sequences can function as enhancers. Mol Reprod Dev 83:541–557CrossRefPubMedGoogle Scholar
  24. Zhang C, Gao L, Xu EY (2016) LncRNA, a new component of expanding RNA-protein regulatory network important for animal sperm development. Semin Cell Dev Biol 59:110–117CrossRefPubMedGoogle Scholar
  25. Zhou W, Shao H, Zhang D, Dong J, Cheng W, Wang L, Teng Y, Yu Z (2015) PTEN signaling is required for the maintenance of spermatogonial stem cells in mouse, by regulating the expressions of PLZF and UTF1. Cell Biosci 5:42CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesBengbu Medical CollegeBengbuPeople’s Republic of China

Personalised recommendations