MicroRNA-122 influences the development of sperm abnormalities from human induced pluripotent stem cells by regulating TNP2 expression

Stem Cells and Development

Volumn 22, Issue 12, 2013, Pages 1839-1850

  Liu, Te ^a,b,c   Huang, Yongyi ^d   Liu, Jianjun ^e   Zhao, Yanhui ^f   Jiang, Lizhen ^d,g   Huang, Qin ^d,g   Cheng, Weiwei ^a   Guo, Lihe ^d,g  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b DONGHUA UNIVERSITY   (China)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^d Sino America United Stem Cell Research Center   (China)

^e Shanghai Second People's Hospital   (China)

^f SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^g INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; MICRORNA 122; PROTAMINE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA CONTENT; FLOW CYTOMETRY; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HAPLOIDY; HUMAN; HUMAN CELL; MALE INFERTILITY; PATHOGENESIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMEN ABNORMALITY; SPERMATOGENESIS; TNP2 GENE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; EMBRYOID BODIES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MICE, SCID; MICRORNAS; MUTATION; PROTAMINES; RNA, MESSENGER; SPERMATOZOA; TERATOMA; TRANSFECTION;

EID: 84881098033     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0653     Document Type: Article

References (47)

1. Miyagawa Y, H Nishimura, A Tsujimura, Y Matsuoka, K Matsumiya, A Okuyama, Y Nishimune and H Tanaka. (2005). Single-nucleotide polymorphisms and mutation analyses of the TNP1 and TNP2 genes of fertile and infertile human male populations. J Androl 26:779-786.
2. Zenzmaier C, R Gerth, M Gruschwitz, H Lindner, E Plas and P Berger. (2011). Decreased levels of genuine large free hCG alpha in men presenting with abnormal semen analysis. Reprod Biol Endocrinol 9:114.
3. Hu W, H Yang, J Sun, Q Zhang, J Yang, L Lu, J Zhang, Y Qin, Y Xia and X Wang. (2011). Polymorphisms in CYP1B1 modify the risk of idiopathic male infertility with abnormal semen quality. Clin Chim Acta 412:1778-1782.
4. Chatzimeletiou K, A Sioga, L Oikonomou, S Char-alampidou, P Kantartzi, V Zournatzi, D Panidis, DG Goulis, L Papadimas and BC Tarlatzis. (2011). Semen analysis by electron and fluorescence microscopy in a case of partial hydatidiform mole reveals a high incidence of abnormal morphology, diploidy, and tetraploidy. Fertil Steril 95: 2430.e1.
5. Moretti E, C Castellini, E Mourvaki, S Capitani, M Geminiani, T Renieri and G Collodel. (2011) Distribution of alpha-and delta-tocopherols in seminal plasma and sperm fractions of men with normal and abnormal semen parameters. J Androl 32:232-239.
6. Kowalczuk CI, RD Saunders and HR Stapleton. (1983). Sperm count and sperm abnormality in male mice after exposure to 2.45 GHz microwave radiation. Mutat Res 122:155-161.
7. Tseden K, O Topaloglu, A Meinhardt, A Dev, I Adham, C Muller, S Wolf, D Bohm, G Schluter, W Engel and K Nayernia. (2007). Premature translation of transition protein 2 mRNA causes sperm abnormalities and male infertility. Mol Reprod Dev 74:273-279.
8. Shirley CR, S Hayashi, S Mounsey, R Yanagimachi and ML Meistrich. (2004). Abnormalities and reduced reproductive potential of sperm from Tnp1-and Tnp2-null double mutant mice. Biol Reprod 71:1220-1229.
9. Liu TD, BY Yu, FH Luo, XL Zhang, SC Wu, LH Liu and YJ Wu. (2011). Gene expression profiling of rat testis development during the early post-natal stages. Reprod Domest Anim 47:724-731.
10. Aoki VW, GL Christensen, JF Atkins and DT Carrell. (2006). Identification of novel polymorphisms in the nuclear protein genes and their relationship with human sperm protamine deficiency and severe male infertility. Fertil Steril 86:1416-1422.
11. Pradeepa MM and MR Rao. (2007). Chromatin remodeling during mammalian spermatogenesis: role of testis specific histone variants and transition proteins. Soc Reprod Fertil Suppl 63:1-10.
12. Chioccarelli T, G Cacciola, L Altucci, SE Lewis, L Simon, G Ricci, C Ledent, R Meccariello, S Fasano, R Pierantoni and G Cobellis. (2010). Cannabinoid receptor 1 influences chromatin remodeling in mouse spermatids by affecting content of transition protein 2 mRNA and histone displacement. Endocrinology 151:5017-5029.
13. Bizzaro D, GC Manicardi, PG Bianchi, U Bianchi, E Mar-iethoz and D Sakkas. (1998). In-situ competition between protamine and fluorochromes for sperm DNA. Mol Hum Reprod 4:127-132.
14. Becker S, Y Soffer, LM Lewin, L Yogev, L Shochat and R Golan. (2008). Spermiogenesis defects in human: detection of transition proteins in semen from some infertile men. An-drologia 40:203-208.
15. Zhao M, CR Shirley, S Mounsey and ML Meistrich. (2004). Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and Tnp2 mutations. Biol Reprod 71:1016-1025.
16. Zhao XY, W Li, Z Lv, L Liu, M Tong, T Hai, J Hao, CL Guo, QW Ma, et al. (2009). iPS cells produce viable mice through tetraploid complementation. Nature 461:86-90.
17. Balhorn R. (2007). The protamine family of sperm nuclear proteins. Genome Biol 8:227.
18. Roque A, I Ponte and P Suau. (2011). Secondary structure of protamine in sperm nuclei: an infrared spectroscopy study. BMC Struct Biol 11:14.
19. Liu T, W Cheng, Y Gao, H Wang and Z Liu. (2012). Mi-croarray analysis of microRNA expression patterns in the semen of infertile men with semen abnormalities. Mol Med Report 6:535-542.
20. Dai L, CH Tsai-Morris, H Sato, J Villar, JH Kang, J Zhang and ML Dufau. (2011). Testis-specific miRNA-469 up-regulated in gonadotropin-regulated testicular RNA helicase (GRTH/DDX25)-null mice silences transition protein 2 and protamine 2 messages at sites within coding region: implications of its role in germ cell development. J Biol Chem 286:44306-44318.
21. Yu Z, T Raabe and NB Hecht. (2005). MicroRNA Mir-n122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod 73:427-433.
22. Yu Z and NB Hecht. (2008). The DNA/RNA-binding protein, translin, binds microRNA122a and increases its in vivo stability. J Androl 29:572-579.
23. Wu S, S Huang, J Ding, Y Zhao, L Liang, T Liu, R Zhan and X He. (2010). Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3¢ untranslated region. Oncogene 29:2302-2308.
24. Cheng W, T Liu, F Jiang, C Liu, X Zhao, Y Gao, H Wang and Z Liu. (2011). microRNA-155 regulates angiotensin II type 1 receptor expression in umbilical vein endothelial cells from severely pre-eclamptic pregnant women. Int J Mol Med 27:393-399.
25. Zhang L, T Liu, Y Huang and J Liu. (2011). microRNA-182 inhibits the proliferation and invasion of human lung ade-nocarcinoma cells through its effect on human cortical actin-associated protein. Int J Mol Med 28:381-388.
26. Cheng W, T Liu, X Wan, Y Gao and H Wang. (2012). Mi-croRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. FEBS J 279:2047-2059.
27. Liu T, W Cheng, Y Huang, Q Huang, L Jiang and L Guo. (2011). Human amniotic epithelial cell feeder layers maintain human iPS cell pluripotency via inhibited endogenous microRNA-145 and increased Sox2 expression. Exp Cell Res 318:424-434.
28. Liu T, G Zou, Y Gao, X Zhao, H Wang, Q Huang, L Jiang, L Guo and W Cheng. (2012). High efficiency of reprogramming CD34(+) cells derived from human amniotic fluid into induced pluripotent stem cells with Oct4. Stem Cells Dev 21:2322-2332.
29. Lee JH, HJ Kim, H Kim, SJ Lee and MC Gye. (2006). In vitro spermatogenesis by three-dimensional culture of rat testic-ular cells in collagen gel matrix. Biomaterials 27:2845-2853.
30. Hayashi K, H Ohta, K Kurimoto, S Aramaki and M Saitou. (2011). Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519-532.
31. Easley CAt, BT Phillips, MM McGuire, JM Barringer, H Valli, BP Hermann, CR Simerly, A Rajkovic, T Miki, KE Orwig and GP Schatten. (2012). Direct differentiation of human pluripotent stem cells into haploid spermatogenic cells. Cell Rep 2:440-446.
32. Yu Z, P Ji, J Cao, S Zhu, Y Li, L Zheng, X Chen and L Feng. (2009). Dazl promotes germ cell differentiation from embryonic stem cells. J Mol Cell Biol 1:93-103.
33. Liu T, Q Chen, Y Huang, Q Huang, L Jiang and L Guo. (2012). Low microRNA-199a expression in human amniotic epithelial cell feeder layers maintains human-induced plu-ripotent stem cell pluripotency via increased leukemia inhibitory factor expression. Acta Biochim Biophys Sin (Shanghai) 44:197-206.
34. Gan CS, PK Chong, TK Pham and PC Wright. (2007). Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Pro-teome Res 6:821-827.
35. Chong PK, H Lee, J Zhou, SC Liu, MC Loh, TT Wang, SP Chan, DT Smoot, H Ashktorab, et al. (2010). ITIH3 is a potential biomarker for early detection of gastric cancer. J Proteome Res 9:3671-3679.
36. Chong PK, CS Gan, TK Pham and PC Wright. (2006). Iso-baric tags for relative and absolute quantitation (iTRAQ) reproducibility: Implication of multiple injections. J Pro-teome Res 5:1232-1240.
37. Pham TK, P Sierocinski, J van der Oost and PC Wright. (2010). Quantitative proteomic analysis of Sulfolobus solfa-taricus membrane proteins. J Proteome Res 9:1165-1172.
38. Han CL, CW Chien, WC Chen, YR Chen, CP Wu, H Li and YJ Chen. (2008). A multiplexed quantitative strategy for membrane proteomics: opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease. Mol Cell Proteomics 7:1983-1997.
39. Ye H, L Sun, X Huang, P Zhang and X Zhao. (2010). A proteomic approach for plasma biomarker discovery with 8-plex iTRAQ labeling and SCX-LC-MS/MS. Mol Cell Bio-chem 343:91-99.
40. Xiao Z, G Li, Y Chen, M Li, F Peng, C Li, F Li, Y Yu, Y Ouyang and Z Chen. (2010). Quantitative proteomic analysis of formalin-fixed and paraffin-embedded nasopharyngeal carcinoma using iTRAQ labeling, two-dimensional liquid chromatography, and tandem mass spectrometry. J His-tochem Cytochem 58:517-527.
41. Dean RA and CM Overall. (2007). Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate de-gradome. Mol Cell Proteomics 6:611-623.
42. Datta A, JE Park, X Li, H Zhang, ZS Ho, K Heese, SK Lim, JP Tam and SK Sze. (2010). Phenotyping of an in vitro model of ischemic penumbra by iTRAQ-based shotgun quantitative proteomics. J Proteome Res 9:472-484.
43. Bantscheff M, M Boesche, D Eberhard, T Matthieson, G Sweetman and B Kuster. (2008). Robust and sensitive iTRAQ quantification on an LTQ Orbitrap mass spectrometer. Mol Cell Proteomics 7:1702-1713.
44. Khattri A, SS Bhushan, V Sireesha, NJ Gupta, BN Chakra-varty, M Deendayal, S Prasad, L Singh and K Thangaraj. (2011). The TNP1 haplotype-GCG is associated with azo-ospermia. Int J Androl 34:173-182.
45. Liu T, Y Huang, L Guo, W Cheng and G Zou. (2012). CD44+/CD105+ human amniotic fluid mesenchymal stem cells survive and proliferate in the ovary long-term in a mouse model of chemotherapy-induced premature ovarian failure. Int J Med Sci 9:592-602.
46. Huang LS, E Voyiaziakis, DF Markenson, KA Sokol, T Hayek and JL Breslow. (1995). apo B gene knockout in mice results in embryonic lethality in homozygotes and neural tube defects, male infertility, and reduced HDL cholesterol ester and apo A-I transport rates in heterozygotes. J Clin Invest 96:2152-2161.
47. Peterlin B, B Zorn, M Volk and T Kunej. (2006). Association between the apolipoprotein B signal peptide gene insertion/deletion polymorphism and male infertility. Mol Hum Re-prod 12:777-779.