Repression of the soma-specific transcriptome by polycomb-repressive complex 2 promotes male germ cell development

Genes and Development

Volumn 28, Issue 18, 2014, Pages 2056-2069

  Mu, Weipeng ^a   Starmer, Joshua ^a   Fedoriw, Andrew M ^a   Yee, Della ^a   Magnuson, Terry ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Epigenetic repression; Gene expression; Meiosis; Polycomb group proteins; Spermatogenesis; Spermatogonia

Indexed keywords

ARF PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; LAMIN; NUCLEAR PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; SUN1 PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; POLYCOMB GROUP PROTEIN;

ANIMAL CELL; ARTICLE; CELL MATURATION; CELL MUTANT; CELL NUCLEUS MEMBRANE; CHROMOSOME ABERRATION; CHROMOSOME PAIRING; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; GENE REPRESSION; GERM CELL DEVELOPMENT; HOMEOSTASIS; MALE; MEIOSIS; MITOSIS; MUTAGENESIS; NONHUMAN; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; TRANSCRIPTION REGULATION; ANIMAL; CELL DIFFERENTIATION; CHROMOSOME; CYTOLOGY; EPIGENETIC REPRESSION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; MALE INFERTILITY; METABOLISM; MOUSE;

EPIGENETIC REPRESSION; GENE EXPRESSION; MEIOSIS; POLYCOMB GROUP PROTEINS; SPERMATOGENESIS; SPERMATOGONIA;

ANIMALS; CELL DIFFERENTIATION; CHROMOSOMES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; INFERTILITY, MALE; LAMINS; MALE; MEIOSIS; MICE; POLYCOMB REPRESSIVE COMPLEX 2; SPERMATOCYTES; TRANSCRIPTOME;

EID: 84907150633     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.246124.114     Document Type: Article

References (62)

1. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K. 2007. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731-734.
2. Aldiri I, Vetter ML. 2012. PRC2 during vertebrate organogenesis: a complex in transition. Dev Biol 367: 91-99.
3. Anders S, Pyl PT, Huber W. 2014. HTSeq— a Python framework to work with high-throughput sequencing data. bioRxiv doi: 10.1101/002824
4. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC. 2008. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci 105: 14976-14980.
5. Aoki R, Chiba T, Miyagi S, Negishi M, Konuma T, Taniguchi H, Ogawa M, Yokosuka O, Iwama A. 2010. The polycomb group gene product Ezh2 regulates proliferation and differentiation of murine hepatic stem/progenitor cells. J Hepatol 52: 854-863.
6. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
7. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini- Otero RD. 2013. Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 24: 196-205.
8. Bowles J, Koopman P. 2007. Retinoic acid, meiosis and germ cell fate in mammals. Development 134: 3401-3411.
9. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, et al. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
10. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, Beekman C, Theilgaard-Monch K, Minucci S, Porse BT, Marine JC, et al. 2007. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 21: 525-530.
11. Branciforte D, Martin SL. 1994. Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol Cell Biol 14: 2584-2592.
12. Britten RJ, Kohne DE. 1968. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science 161: 529-540.
13. Burke B, Stewart CL. 2013. The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14: 13-24.
14. Calabrese JM, Sun W, Song L, Mugford JW, Williams L, Yee D, Starmer J, Mieczkowski P, Crawford GE, Magnuson T. 2012. Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151: 951-963.
15. Chandler RL, Chandler KJ, McFarland KA, Mortlock DP. 2007. Bmp2 transcription in osteoblast progenitors is regulated by a distant 3' enhancer located 156.3 kilobases from the promoter. Mol Cell Biol 27: 2934-2951.
16. Chang YF, Lee-Chang JS, Panneerdoss S, MacLean JA2nd, Rao MK. 2011. Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis. Biotechniques 51: 341-342, 344.
17. Churchman ML, Roig I, Jasin M, Keeney S, Sherr CJ. 2011. Expression of arf tumor suppressor in spermatogonia facilitates meiotic progression in male germ cells. PLoS Genet 7: e1002157.
18. Commerford SL, Carsten AL, Cronkite EP. 1982. Histone turnover within nonproliferating cells. Proc Natl Acad Sci 79: 1163-1165.
19. Delgado-Olguin P, Huang Y, Li X, Christodoulou D, Seidman CE, Seidman JG, Tarakhovsky A, Bruneau BG. 2012. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat Genet 44: 343-347.
20. Dernburg AF. 2013. Pushing the (nuclear) envelope into meiosis. Genome Biol 14: 110.
21. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M. 2007. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12: 863-872.
22. Dreesen O, Chojnowski A, Ong PF, Zhao TY, Common JE, Lunny D, Lane EB, Lee SJ, Vardy LA, Stewart CL, et al. 2013. Lamin B1 fluctuations have differential effects on cellular proliferation and senescence. J Cell Biol 200: 605-617.
23. Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su IH, Hannon G, Tarakhovsky A, Fuchs E. 2009. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 136: 1122-1135.
24. Ezhkova E, Lien WH, Stokes N, Pasolli HA, Silva JM, Fuchs E. 2011. EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev 25: 485-498.
25. Fedoriw AM, Calabrese JM, Mu W, Yee D, Magnuson T. 2012. Differentiation-driven nucleolar association of the mouse imprinted Kcnq1 locus. G3 2: 1521-1528.
26. Feng J, Liu T, Qin B, Zhang Y, Liu XS. 2012. Identifying ChIP-seq enrichment using MACS. Nat Protoc 7: 1728-1740.
27. Gallardo T, Shirley L, John GB, Castrillon DH. 2007. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45: 413-417.
28. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S. 2006. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26: 3738-3751.
29. Hiraoka Y, Dernburg AF. 2009. The SUN rises on meiotic chromosome dynamics. Dev Cell 17: 598-605.
30. Ishiguro K, Kim J, Shibuya H, Hernandez-Hernandez A, Suzuki A, Fukagawa T, Shioi G, Kiyonari H, Li XC, Schimenti J, et al. 2014. Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev 28: 594-607.
31. Jahn D, Schramm S, Benavente R, Alsheimer M. 2010. Dynamic properties of meiosis-specific lamin C2 and its impact on nuclear envelope integrity. Nucleus 1: 273-283.
32. Juan AH, Derfoul A, Feng X, Ryall JG, Dell'Orso S, Pasut A, Zare H, Simone JM, Rudnicki MA, Sartorelli V. 2011. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev 25: 789-794.
33. Kotake Y, Cao R, Viatour P, Sage J, Zhang Y, Xiong Y. 2007. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4a tumor suppressor gene. Genes Dev 21: 49-54.
34. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. 2006. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci 103: 2474-2479.
35. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
36. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, et al. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
37. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A. 2010. Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev 24: 265-276.
38. Liebe B, Petukhova G, Barchi M, Bellani M, Braselmann H, Nakano T, Pandita TK, Jasin M, Fornace A, Meistrich ML, et al. 2006. Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp Cell Res 312: 3768-3781.
39. Link J, Jahn D, Schmitt J, Gob E, Baar J, Ortega S, Benavente R, Alsheimer M. 2013. The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet 9: e1003261.
40. Liu P, Jenkins NA, Copeland NG. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13: 476-484.
41. Mahadevaiah SK, Costa Y, Turner JM. 2009. Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol Biol 558: 433-444.
42. Montgomery ND, Yee D, Chen A, Kalantry S, Chamberlain SJ, Otte AP, Magnuson T. 2005. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15: 942-947.
43. Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, Watanabe Y. 2012. A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 198: 165-172.
44. Ostlund C, Folker ES, Choi JC, Gomes ER, Gundersen GG, Worman HJ. 2009. Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci 122: 4099-4108.
45. Patel T, Tursun B, Rahe DP, Hobert O. 2012. Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types. Cell Reports 2: 1178-1186.
46. Peters AH, Plug AW, van Vugt MJ, de Boer P. 1997. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66-68.
47. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
48. Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, Bradley A, de Rooij DG, Burgoyne PS, Turner JM. 2010. Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol 20: 2117-2123.
49. Sasaki H, Matsui Y. 2008. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129-140.
50. Scherthan H. 2009. Analysis of telomere dynamics in mouse spermatogenesis. Methods Mol Biol 558: 383-399.
51. Schlecht U, Demougin P, Koch R, Hermida L, Wiederkehr C, Descombes P, Pineau C, Jegou B, Primig M. 2004. Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Mol Biol Cell 15: 1031-1043.
52. Schutz W, Benavente R, Alsheimer M. 2005. Dynamic properties of germ line-specific lamin B3: the role of the shortened rod domain. Eur J Cell Biol 84: 649-662.
53. Shen L, Shao N, Liu X, Nestler E. 2014. ngs.plot: quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 15: 284.
54. Shima JE, McLean DJ, McCarrey JR, Griswold MD. 2004. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 71: 319-330.
55. Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, de Boer P, Bortvin A. 2008. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285-297.
56. Stuurman N, Delbecque JP, Callaerts P, Aebi U. 1999. Ectopic overexpression of Drosophila lamin C is stage-specific lethal. Exp Cell Res 248: 350-357.
57. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102: 15545-15550.
58. Wang J, Mager J, Chen Y, Schneider E, Cross JC, Nagy A, Magnuson T. 2001. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 28: 371-375.
59. Wynne DJ, Rog O, Carlton PM, Dernburg AF. 2012. Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 196: 47-64.
60. Yokobayashi S, Liang CY, Kohler H, Nestorov P, Liu Z, Vidal M, van Lohuizen M, Roloff TC, Peters AH. 2013. PRC1 coordinates timing of sexual differentiation of female primordial germ cells. Nature 495: 236-240.
61. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y. 2006. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 133: 1495-1505.
62. Yuan W, Leisner TM, McFadden AW, Clark S, Hiller S, Maeda N, O'Brien DA, Parise LV. 2006. CIB1 is essential for mouse spermatogenesis. Mol Cell Biol 26: 8507-8514.