Mettl3-/Mettl14-mediated mRNA N 6-methyladenosine modulates murine spermatogenesis

Cell Research

Volumn 27, Issue 10, 2017, Pages 1216-1230

  Lin, Zhen ^a   Hsu, Phillip J ^b   Xing, Xudong ^c   Fang, Jianhuo ^c   Lu, Zhike ^b   Zou, Qin ^c   Zhang, Ke Jia ^a   Zhang, Xiao ^d   Zhou, Yuchuan ^a   Zhang, Teng ^a   Zhang, Youcheng ^a   Song, Wanlu ^c   Jia, Guifang ^d   Yang, Xuerui ^c   He, Chuan ^b,d   Tong, Ming Han ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF CHICAGO   (United States)

^c Tsinghua University   (China)

^d PEKING UNIVERSITY   (China)

Author keywords

m6A RNA modifcation; Mettl14; Mettl3; spermatogonial stem cell; spermiogenesis

Indexed keywords

ADENOSINE; MESSENGER RNA; METHYLTRANSFERASE; METTL14 PROTEIN, MOUSE; METTL3 PROTEIN, MOUSE; N(6)-METHYLADENOSINE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STRA8 PROTEIN, MOUSE;

ANALOGS AND DERIVATIVES; ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOUSE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; STEM CELL; TESTIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; METHYLTRANSFERASES; MICE; RNA, MESSENGER; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; SPERMATOZOA; STEM CELLS; TESTIS;

EID: 85030687382     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2017.117     Document Type: Article

References (70)

1. Griswold MD. Spermatogenesis: the commitment to meiosis. Physiol Rev 2016; 96: 1-17.
2. Clermont Y. Kinetics of spermatogenesis in mammals: semi-niferous epithelium cycle and spermatogonial renewal. Physi-ol Rev 1972; 52: 198-236.
3. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008; 24: 263-286.
4. Kleene KC. Connecting cis-elements and trans-factors with mechanisms of developmental regulation of mRNA translation in meiotic and haploid mammalian spermatogenic cells. Reproduction 2013; 146:R1-R19.
5. Alarcon CR, Goodarzi H, Lee H, Liu X, Tavazoie S, Tavazoie SF. HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA processing events. Cell 2015; 162:1299-1308.
6. Dominissini D, Moshitch-Moshkovitz S, Schwartz S, et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012; 485:201-206.
7. Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 2012; 149:1635-1646.
8. 6-methyladenosine modulates messenger RNA translation effciency. Cell 2015; 161:1388-1399.
9. Wei CM, Gershowitz A, Moss B. Methylated nucleotides block 5′ terminus of HeLa cell messenger RNA. Cell 1975; 4:379-386.
10. 6-methyladenosine-depen-dent regulation of messenger RNA stability. Nature 2014; 505:117-120.
11. 6A mRNA methylation directs translational control of heat shock response. Nature 2015; 526:591-594.
12. 6A methylation regulates the ultraviolet-induced DNA damage response. Nature 2017; 543:573-576.
13. Fustin JM, Doi M, Yamaguchi Y, et al. RNA-methylation-de-pendent RNA processing controls the speed of the circadian clock. Cell 2013; 155:793-806.
14. 6A-dependent mater-nal mRNA clearance facilitates zebrafsh maternal-to-zygotic transition. Nature 2017; 542:475-478.
15. 6A Demethylase ALKBH5 maintains tumorigenicity of glioblastoma stem-like cells by sustaining FOXM1 expression and cell proliferation program. Cancer Cell 2017; 31:591-606 e596.
16. 6A RNA methylation regulates the self-renewal and tumorigenesis of glioblastoma stem cells. Cell Rep 2017; 18:2622-2634.
17. 6A meth-yltransferase METTL3 promotes translation in human cancer cells. Mol Cell 2016; 62:335-345.
18. 6-adenosine)-methyltransfer-ase. RNA 1997; 3:1233-1247.
19. 6-adenosine methylation. Nat Chem Biol 2014; 10:93-95.
20. 6-methyladenosine methyltrans-ferase. Cell Res 2014; 24:177-189.
21. 6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 2011; 7:885-887.
22. Zheng G, Dahl JA, Niu Y, et al. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 2013; 49:18-29.
23. 6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science 2015; 347:1002-1006.
24. 6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat Cell Biol 2014; 16:191-198.
25. 6A potentiates Sxl alternative pre-mRNA splicing for robust Drosophila sex determination. Nature 2016; 540:301-304.
26. 6A modulates neuronal functions and sex determination in Drosophila. Nature 2016; 540:242-247.
27. Hongay CF, Orr-Weaver TL. Drosophila inducer of MEiosis 4 (IME4) is required for Notch signaling during oogenesis. Proc Natl Acad Sci USA 2011; 108:14855-14860.
28. Schwartz S, Agarwala SD, Mumbach MR, et al. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 2013; 155:1409-1421.
29. Gallardo T, Shirley L, John GB, Castrillon DH. Generation of a germ cell-specifc mouse transgenic Cre line, Vasa-Cre. Genesis 2007; 45:413-417.
30. Roundtree IA, Evans ME, Pan T, He C. Dynamic RNA modi-fcations in gene expression regulation. Cell 2017; 169:1187-1200.
31. 6-adenos-ine methylation by the METTL3-METTL14 complex. Nature 2016; 534:575-578.
32. 6-methyladenosine in mRNA: a potential mech-anism for the activity of the IME4 gene. Nucleic Acids Res 2002; 30:4509-4518.
33. Shah JC, Clancy MJ. IME4, a gene that mediates MAT and nutritional control of meiosis in Saccharomyces cerevisiae. Mol Cell Biol 1992; 12:1078-1086.
34. Agarwala SD, Blitzblau HG, Hochwagen A, Fink GR. RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLoS Genet 2012; 8:e1002732.
35. 6A methyltransferase METTL16 regulates SAM synthetase in-tron retention. Cell 2017; 169:824-835 e814.
36. Shirakawa T, Yaman-Deveci R, Tomizawa S, et al. An epigen-etic switch is crucial for spermatogonia to exit the undifferen-tiated state toward a Kit-positive identity. Development 2013; 140:3565-3576.
37. Goertz MJ, Wu Z, Gallardo TD, Hamra FK, Castrillon DH. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 2011; 121:3456-3466.
38. Chan F, Oatley MJ, Kaucher AV, et al. Functional and molecular features of the Id4+ germline stem cell population in mouse testes. Genes Dev 2014; 28:1351-1362.
39. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM. Differential expression of c-kit in mouse undifferentiat-ed and differentiating type A spermatogonia. Endocrinology 1999; 140:5894-5900.
40. Wang M, Guo Y, Wang M, et al. The glial cell-derived neuro-trophic factor (GDNF)-responsive phosphoprotein landscape identifes raptor phosphorylation required for spermatogonial progenitor cell proliferation. Mol Cell Proteomics 2017; 16:982-997.
41. Hao J, Yamamoto M, Richardson TE, et al. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008; 26:1587-1597.
42. Laronda MM, Jameson JL. Sox3 functions in a cell-autonomous manner to regulate spermatogonial differentiation in mice. Endocrinology 2011; 152:1606-1615.
43. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL. Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 2003; 23:8084-8091.
44. Oatley JM, Kaucher AV, Avarbock MR, Brinster RL. Regulation of mouse spermatogonial stem cell differentiation by STAT3 signaling. Biol Reprod 2010; 83:427-433.
45. Zhou Q, Li Y, Nie R, et al. Expression of stimulated by reti-noic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol Re-prod 2008; 78:537-545.
46. Zhou Q, Nie R, Li Y, et al. Expression of stimulated by ret-inoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-suffcient postnatal murine testes. Biol Reprod 2008; 79:35-42.
47. Buaas FW, Kirsh AL, Sharma M, et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36:647-652.
48. Costoya JA, Hobbs RM, Barna M, et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653-659.
49. Wang H, Zhao R, Guo C, et al. Knockout of BRD7 results in impaired spermatogenesis and male infertility. Sci Rep 2016; 6:21776.
50. Dass B, Tardif S, Park J Y, et al. Loss of polyadenylation protein tauCstF-64 causes spermatogenic defects and male infertility. Proc Natl Acad Sci USA 2007; 104:20374-20379.
51. Kuroki S, Akiyoshi M, Tokura M, et al. JMJD1C, a JmjC domain-containing protein, is required for long-term maintenance of male germ cells in mice. Biol Reprod 2013; 89:93.
52. Meyer-Ficca ML, Ihara M, Bader JJ, Leu NA, Beneke S, Meyer RG. Spermatid head elongation with normal nuclear shaping requires ADP-ribosyltransferase PARP11 (ARTD11) in mice. Biol Reprod 2015; 92:80.
53. Kawa S, Ito C, Toyama Y, et al. Azoospermia in mice with targeted disruption of the Brek/Lmtk2 (brain-enriched kinase/lemur tyrosine kinase 2) gene. Proc Natl Acad Sci USA 2006; 103:19344-19349.
54. Pandey RR, Tokuzawa Y, Yang Z, et al. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc Natl Acad Sci USA 2013; 110:16492-16497.
55. Cao Y, Fu YL, Ge CH, et al. Mice overexpression of human augmenter of liver regeneration (hALR) in male germ cells shows abnormal spermatogenesis and reduced fertility. Endo-cr J 2012; 59:989-999.
56. Tong MH, Mitchell DA, McGowan SD, Evanoff R, Gris-wold MD. Two miRNA clusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of sper-matogonial differentiation in mice. Biol Reprod 2012; 86:72.
57. Hogarth CA, Evanoff R, Mitchell D, et al. Turning a sper-matogenic wave into a tsunami: synchronizing murine sper-matogenesis using WIN 18, 446. Biol Reprod 2013; 88:40.
58. Gaysinskaya V, Soh IY, van der Heijden GW, Bortvin A. Optimized flow cytometry isolation of murine spermatocytes. Cytometry A 2014; 85:556-565.
59. Chen Y, Ma L, Hogarth C, Wei G, Griswold MD, Tong MH. Retinoid signaling controls spermatogonial differentiation by regulating expression of replication-dependent core histone genes. Development 2016; 143:1502-1511.
60. Anders S, Pyl PT, Huber W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 2015; 31:166-169.
61. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013; 14:R36.
62. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Biocon-ductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139-140.
63. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS. The ribosome profling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 2012; 7:1534-1550.
64. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profling. Science 2009; 324:218-223.
65. Xiao Z, Zou Q, Liu Y, Yang X. Genome-wide assessment of differential translations with ribosome profling data. Nat Commun 2016; 7:11194.
66. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 2011; 17:10-12.
67. Crappe J, Ndah E, Koch A, et al. PROTEOFORMER: deep proteome coverage through ribosome profling and MS integration. Nucleic Acids Res 2015; 43:e29.
68. Ingolia NT, Brar GA, Stern-Ginossar N, et al. Ribosome pro-fling reveals pervasive translation outside of annotated protein-coding genes. Cell Rep 2014; 8:1365-1379.
69. Ingolia NT, Lareau LF, Weissman JS. Ribosome profling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011; 147:789-802.
70. Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 2011; 6:e21800.