Meiotic cohesins mediate initial loading of HORMAD1 to the chromosomes and coordinate SC formation during meiotic prophase
Autoři:
Yasuhiro Fujiwara aff001; Yuki Horisawa-Takada aff002; Erina Inoue aff001; Naoki Tani aff003; Hiroki Shibuya aff004; Sayoko Fujimura aff003; Ryo Kariyazono aff005; Toyonori Sakata aff006; Kunihiro Ohta aff005; Kimi Araki aff007; Yuki Okada aff001; Kei-ichiro Ishiguro aff002
Působiště autorů:
Laboratory of Pathology and Development, Institute for Quantitative Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan
aff001; Department of Chromosome Biology, Institute of Molecular Embryology and Genetics, Kumamoto University, Chuo-ku, Kumamoto, Japan
aff002; Liaison Laboratory Research Promotion Center, IMEG, Kumamoto University, Kumamoto, Japan
aff003; Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
aff004; Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Meguro-ku, Tokyo, Japan
aff005; Laboratory of Genome Structure and Function, the Institute for Quantitative Biosciences, University of Tokyo, Bunkyo, Tokyo, Japan
aff006; Institute of Resource Development and Analysis & Center for Metabolic Regulation of Healthy Aging, Kumamoto University, Kumamoto, Japan
aff007
Vyšlo v časopise:
Meiotic cohesins mediate initial loading of HORMAD1 to the chromosomes and coordinate SC formation during meiotic prophase. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009048
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009048
Souhrn
During meiotic prophase, sister chromatids are organized into axial element (AE), which underlies the structural framework for the meiotic events such as meiotic recombination and homolog synapsis. HORMA domain-containing proteins (HORMADs) localize along AE and play critical roles in the regulation of those meiotic events. Organization of AE is attributed to two groups of proteins: meiotic cohesins REC8 and RAD21L; and AE components SYCP2 and SYCP3. It has been elusive how these chromosome structural proteins contribute to the chromatin loading of HORMADs prior to AE formation. Here we newly generated Sycp2 null mice and showed that initial chromatin loading of HORMAD1 was mediated by meiotic cohesins prior to AE formation. HORMAD1 interacted not only with the AE components SYCP2 and SYCP3 but also with meiotic cohesins. Notably, HORMAD1 interacted with meiotic cohesins even in Sycp2-KO, and localized along cohesin axial cores independently of the AE components SYCP2 and SYCP3. Hormad1/Rad21L-double knockout (dKO) showed more severe defects in the formation of synaptonemal complex (SC) compared to Hormad1-KO or Rad21L-KO. Intriguingly, Hormad1/Rec8-dKO but not Hormad1/Rad21L-dKO showed precocious separation of sister chromatid axis. These findings suggest that meiotic cohesins REC8 and RAD21L mediate chromatin loading and the mode of action of HORMAD1 for synapsis during early meiotic prophase.
Klíčová slova:
Chromatids – Chromatin – Chromosome staining – Immunoprecipitation – Meiotic prophase – Spermatocytes – Synapsis – Testes
Zdroje
1. Bhalla N, Dernburg AF. Prelude to a division. Annu Rev Cell Dev Biol. 2008;24:397–424. Epub 2008/07/04. doi: 10.1146/annurev.cellbio.23.090506.123245 18597662
2. Barzel A, Kupiec M. Finding a match: how do homologous sequences get together for recombination? Nat Rev Genet. 2008;9(1):27–37. Epub 2007/11/28. doi: 10.1038/nrg2224 18040271.
3. Cahoon CK, Hawley RS. Regulating the construction and demolition of the synaptonemal complex. Nat Struct Mol Biol. 2016;23(5):369–77. Epub 2016/05/05. doi: 10.1038/nsmb.3208 27142324.
4. Keeney S, Lange J, Mohibullah N. Self-organization of meiotic recombination initiation: general principles and molecular pathways. Annu Rev Genet. 2014;48:187–214. Epub 2014/11/26. doi: 10.1146/annurev-genet-120213-092304 25421598
5. Takemoto K, Imai Y, Saito K, Kawasaki T, Carlton PM, Ishiguro KI, et al. Sycp2 is essential for synaptonemal complex assembly, early meiotic recombination and homologous pairing in zebrafish spermatocytes. PLoS Genet. 2020;16(2):e1008640. Epub 2020/02/25. doi: 10.1371/journal.pgen.1008640 32092049.
6. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol. 2006;173(4):497–507. Epub 2006/05/24. doi: 10.1083/jcb.200603063 16717126
7. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, Hoog C. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Molecular Cell. 2000;5(1):73–83. Epub 2000/03/11. doi: 10.1016/s1097-2765(00)80404-9 10678170.
8. Zickler D, Kleckner N. Recombination, Pairing, and Synapsis of Homologs during Meiosis. Cold Spring Harb Perspect Biol. 2015;7(6). Epub 2015/05/20. doi: 10.1101/cshperspect.a016626 25986558
9. Baudat F, Imai Y, de Massy B. Meiotic recombination in mammals: localization and regulation. Nat Rev Genet. 2013;14(11):794–806. doi: 10.1038/nrg3573 24136506.
10. Gerton JL, Hawley RS. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet. 2005;6(6):477–87. doi: 10.1038/nrg1614 15931171.
11. Page SL, Hawley RS. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–58. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851.
12. Ishiguro KI. The cohesin complex in mammalian meiosis. Genes Cells. 2019;24(1):6–30. Epub 2018/11/28. doi: 10.1111/gtc.12652 30479058.
13. Biswas U, Hempel K, Llano E, Pendas A, Jessberger R. Distinct Roles of Meiosis-Specific Cohesin Complexes in Mammalian Spermatogenesis. PLoS Genet. 2016;12(10):e1006389. Epub 2016/10/30. doi: 10.1371/journal.pgen.1006389 27792785
14. Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C. Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol. 2003;160(5):657–70. Epub 2003/03/05. doi: 10.1083/jcb.200212080 12615909
15. Lee J, Iwai T, Yokota T, Yamashita M. Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J Cell Sci. 2003;116(Pt 13):2781–90. Epub 2003/05/22. doi: 10.1242/jcs.00495 12759374.
16. Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y. A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep. 2011;12(3):267–75. doi: 10.1038/embor.2011.2 21274006
17. Lee J, Hirano T. RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol. 2011;192(2):263–76. Epub 2011/01/19. doi: 10.1083/jcb.201008005 21242291
18. Herran Y, Gutierrez-Caballero C, Sanchez-Martin M, Hernandez T, Viera A, Barbero JL, et al. The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J. 2011;30(15):3091–105. doi: 10.1038/emboj.2011.222 21743440
19. Pelttari J, Hoja MR, Yuan L, Liu JG, Brundell E, Moens P, et al. A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells. Mol Cell Biol. 2001;21(16):5667–77. Epub 2001/07/21. doi: 10.1128/MCB.21.16.5667-5677.2001 11463847
20. Kumar R, Ghyselinck N, Ishiguro K, Watanabe Y, Kouznetsova A, Hoog C, et al. MEI4—a central player in the regulation of meiotic DNA double-strand break formation in the mouse. J Cell Sci. 2015;128(9):1800–11. Epub 2015/03/22. doi: 10.1242/jcs.165464 25795304
21. Ishiguro K, Kim J, Shibuya H, Hernandez-Hernandez A, Suzuki A, Fukagawa T, et al. Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev. 2014;28(6):594–607. doi: 10.1101/gad.237313.113 24589552
22. Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell. 2005;8(6):949–61. doi: 10.1016/j.devcel.2005.03.018 15935783.
23. Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC. Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin Rec8. Genesis. 2004;40(3):184–94. Epub 2004/10/30. doi: 10.1002/gene.20085 15515002.
24. Bhattacharyya T, Walker M, Powers NR, Brunton C, Fine AD, Petkov PM, et al. Prdm9 and Meiotic Cohesin Proteins Cooperatively Promote DNA Double-Strand Break Formation in Mammalian Spermatocytes. Curr Biol. 2019;29(6):1002–18 e7. Epub 2019/03/12. doi: 10.1016/j.cub.2019.02.007 30853435.
25. Llano E, Herran Y, Garcia-Tunon I, Gutierrez-Caballero C, de Alava E, Barbero JL, et al. Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol. 2012;197(7):877–85. doi: 10.1083/jcb.201201100 22711701
26. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000;6(5):989–98. doi: 10.1016/s1097-2765(00)00098-8 11106739.
27. Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell. 2000;6(5):975–87. Epub 2000/12/07. doi: 10.1016/s1097-2765(00)00097-6 11106738.
28. Robert T, Nore A, Brun C, Maffre C, Crimi B, Bourbon HM, et al. The TopoVIB-Like protein family is required for meiotic DNA double-strand break formation. Science. 2016;351(6276):943–9. Epub 2016/02/27. doi: 10.1126/science.aad5309 26917764.
29. Vrielynck N, Chambon A, Vezon D, Pereira L, Chelysheva L, De Muyt A, et al. A DNA topoisomerase VI-like complex initiates meiotic recombination. Science. 2016;351(6276):939–43. Epub 2016/02/27. doi: 10.1126/science.aad5196 26917763.
30. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 2009;5(10):e1000702. doi: 10.1371/journal.pgen.1000702 19851446
31. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, et al. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet. 2010;6(11):e1001190. doi: 10.1371/journal.pgen.1001190 21079677
32. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, et al. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol. 2011;13(5):599–610. Epub 2011/04/12. doi: 10.1038/ncb2213 21478856
33. Kogo H, Tsutsumi M, Ohye T, Inagaki H, Abe T, Kurahashi H. HORMAD1-dependent checkpoint/surveillance mechanism eliminates asynaptic oocytes. Genes Cells. 2012;17(6):439–54. doi: 10.1111/j.1365-2443.2012.01600.x 22530760.
34. Kogo H, Tsutsumi M, Inagaki H, Ohye T, Kiyonari H, Kurahashi H. HORMAD2 is essential for synapsis surveillance during meiotic prophase via the recruitment of ATR activity. Genes Cells. 2012;17(11):897–912. Epub 2012/10/09. doi: 10.1111/gtc.12005 23039116.
35. Fukuda T, Daniel K, Wojtasz L, Toth A, Hoog C. A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp Cell Res. 2010;316(2):158–71. Epub 2009/08/19. doi: 10.1016/j.yexcr.2009.08.007 19686734.
36. Stanzione M, Baumann M, Papanikos F, Dereli I, Lange J, Ramlal A, et al. Meiotic DNA break formation requires the unsynapsed chromosome axis-binding protein IHO1 (CCDC36) in mice. Nat Cell Biol. 2016;18(11):1208–20. doi: 10.1038/ncb3417 27723721
37. Kumar R, Oliver C, Brun C, Juarez-Martinez AB, Tarabay Y, Kadlec J, et al. Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4. Life Sci Alliance. 2018;1(6):e201800259. Epub 2018/12/21. doi: 10.26508/lsa.201800259 30569039
38. Imai Y, Baudat F, Taillepierre M, Stanzione M, Toth A, de Massy B. The PRDM9 KRAB domain is required for meiosis and involved in protein interactions. Chromosoma. 2017;126(6):681–95. Epub 2017/05/21. doi: 10.1007/s00412-017-0631-z 28527011
39. Baker CL, Petkova P, Walker M, Flachs P, Mihola O, Trachtulec Z, et al. Multimer Formation Explains Allelic Suppression of PRDM9 Recombination Hotspots. PLoS Genet. 2015;11(9):e1005512. Epub 2015/09/15. doi: 10.1371/journal.pgen.1005512 26368021
40. Grey C, Barthes P, Chauveau-Le Friec G, Langa F, Baudat F, de Massy B. Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol. 2011;9(10):e1001176. Epub 2011/10/27. doi: 10.1371/journal.pbio.1001176 22028627
41. Powers NR, Parvanov ED, Baker CL, Walker M, Petkov PM, Paigen K. The Meiotic Recombination Activator PRDM9 Trimethylates Both H3K36 and H3K4 at Recombination Hotspots In Vivo. PLoS Genet. 2016;12(6):e1006146. Epub 2016/07/01. doi: 10.1371/journal.pgen.1006146 27362481
42. Diagouraga B, Clement JAJ, Duret L, Kadlec J, de Massy B, Baudat F. PRDM9 Methyltransferase Activity Is Essential for Meiotic DNA Double-Strand Break Formation at Its Binding Sites. Mol Cell. 2018;69(5):853–65 e6. Epub 2018/02/27. doi: 10.1016/j.molcel.2018.01.033 29478809.
43. Lange J, Yamada S, Tischfield SE, Pan J, Kim S, Zhu X, et al. The Landscape of Mouse Meiotic Double-Strand Break Formation, Processing, and Repair. Cell. 2016;167(3):695–708 e16. Epub 2016/10/22. doi: 10.1016/j.cell.2016.09.035 27745971
44. Grey C, Clement JA, Buard J, Leblanc B, Gut I, Gut M, et al. In vivo binding of PRDM9 reveals interactions with noncanonical genomic sites. Genome Res. 2017;27(4):580–90. Epub 2017/03/25. doi: 10.1101/gr.217240.116 28336543
45. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell. 2008;132(5):758–70. Epub 2008/03/11. doi: 10.1016/j.cell.2008.01.035 18329363.
46. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell. 2011;146(3):372–83. Epub 2011/08/06. doi: 10.1016/j.cell.2011.07.003 21816273.
47. Miyoshi T, Ito M, Kugou K, Yamada S, Furuichi M, Oda A, et al. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol Cell. 2012;47(5):722–33. Epub 2012/07/31. doi: 10.1016/j.molcel.2012.06.023 22841486.
48. Kariyazono R, Oda A, Yamada T, Ohta K. Conserved HORMA domain-containing protein Hop1 stabilizes interaction between proteins of meiotic DNA break hotspots and chromosome axis. Nucleic Acids Res. 2019;47(19):10166–80. Epub 2019/10/31. doi: 10.1093/nar/gkz754 31665745
49. West AM, Rosenberg SC, Ur SN, Lehmer MK, Ye Q, Hagemann G, et al. A conserved filamentous assembly underlies the structure of the meiotic chromosome axis. Elife. 2019;8. Epub 2019/01/19. doi: 10.7554/eLife.40372 30657449
50. Hogarth CA, Evanoff R, Mitchell D, Kent T, Small C, Amory JK, et al. Turning a spermatogenic wave into a tsunami: synchronizing murine spermatogenesis using WIN 18,446. Biol Reprod. 2013;88(2):40. Epub 2013/01/04. doi: 10.1095/biolreprod.112.105346 23284139
51. Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, Fu J, et al. Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev. 2012;26(9):958–73. Epub 2012/05/03. doi: 10.1101/gad.187559.112 22549958
52. Shin YH, McGuire MM, Rajkovic A. Mouse HORMAD1 is a meiosis i checkpoint protein that modulates DNA double- strand break repair during female meiosis. Biol Reprod. 2013;89(2):29. Epub 2013/06/14. doi: 10.1095/biolreprod.112.106773 23759310
53. Boekhout M, Karasu ME, Wang J, Acquaviva L, Pratto F, Brick K, et al. REC114 Partner ANKRD31 Controls Number, Timing, and Location of Meiotic DNA Breaks. Mol Cell. 2019;74(5):1053–68 e8. Epub 2019/04/21. doi: 10.1016/j.molcel.2019.03.023 31003867
54. Papanikos F, Clement JAJ, Testa E, Ravindranathan R, Grey C, Dereli I, et al. Mouse ANKRD31 Regulates Spatiotemporal Patterning of Meiotic Recombination Initiation and Ensures Recombination between X and Y Sex Chromosomes. Mol Cell. 2019;74(5):1069–85 e11. Epub 2019/04/20. doi: 10.1016/j.molcel.2019.03.022 31000436.
55. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, et al. Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol. 2004;6(6):555–62. Epub 2004/05/18. doi: 10.1038/ncb1135 15146193.
56. Hopkins J, Hwang G, Jacob J, Sapp N, Bedigian R, Oka K, et al. Meiosis-specific cohesin component, Stag3 is essential for maintaining centromere chromatid cohesion, and required for DNA repair and synapsis between homologous chromosomes. PLoS Genet. 2014;10(7):e1004413. doi: 10.1371/journal.pgen.1004413 24992337
57. Fukuda T, Fukuda N, Agostinho A, Hernandez-Hernandez A, Kouznetsova A, Hoog C. STAG3-mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis. EMBO J. 2014;33(11):1243–55. Epub 2014/05/07. doi: 10.1002/embj.201387329 24797475
58. Winters T, McNicoll F, Jessberger R. Meiotic cohesin STAG3 is required for chromosome axis formation and sister chromatid cohesion. EMBO J. 2014;33(11):1256–70. Epub 2014/05/07. doi: 10.1002/embj.201387330 24797474
59. Fukuda T, Pratto F, Schimenti JC, Turner JM, Camerini-Otero RD, Hoog C. Phosphorylation of chromosome core components may serve as axis marks for the status of chromosomal events during mammalian meiosis. PLoS Genet. 2012;8(2):e1002485. Epub 2012/02/22. doi: 10.1371/journal.pgen.1002485 22346761
60. Agostinho A, Manneberg O, van Schendel R, Hernandez-Hernandez A, Kouznetsova A, Blom H, et al. High density of REC8 constrains sister chromatid axes and prevents illegitimate synaptonemal complex formation. EMBO Rep. 2016;17(6):901–13. Epub 2016/05/14. doi: 10.15252/embr.201642030 27170622
61. Unal E, Heidinger-Pauli JM, Koshland D. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science. 2007;317(5835):245–8. Epub 2007/07/14. doi: 10.1126/science.1140637 17626885.
62. Sun X, Huang L, Markowitz TE, Blitzblau HG, Chen D, Klein F, et al. Transcription dynamically patterns the meiotic chromosome-axis interface. Elife. 2015;4. Epub 2015/08/11. doi: 10.7554/eLife.07424 26258962
63. Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F, McFarlane RJ, et al. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci. 2004;117(Pt 15):3343–51. Epub 2004/07/01. doi: 10.1242/jcs.01203 15226405.
64. Mao-Draayer Y, Galbraith AM, Pittman DL, Cool M, Malone RE. Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics. 1996;144(1):71–86. Epub 1996/09/01. 8878674
65. Parvanov ED, Tian H, Billings T, Saxl RL, Spruce C, Aithal R, et al. PRDM9 interactions with other proteins provide a link between recombination hotspots and the chromosomal axis in meiosis. Mol Biol Cell. 2017;28(3):488–99. Epub 2016/12/10. doi: 10.1091/mbc.E16-09-0686 27932493
66. Rinaldi VD, Bolcun-Filas E, Kogo H, Kurahashi H, Schimenti JC. The DNA Damage Checkpoint Eliminates Mouse Oocytes with Chromosome Synapsis Failure. Mol Cell. 2017;67(6):1026–36 e2. Epub 2017/08/29. doi: 10.1016/j.molcel.2017.07.027 28844861
67. Ishiguro KI, Matsuura K, Tani N, Takeda N, Usuki S, Yamane M, et al. MEIOSIN Directs the Switch from Mitosis to Meiosis in Mammalian Germ Cells. Dev Cell. 2020;52(4):429–45 e10. Epub 2020/02/08. doi: 10.1016/j.devcel.2020.01.010 32032549.
68. Sullivan BA. Optical mapping of protein-DNA complexes on chromatin fibers. Methods Mol Biol. 2010;659:99–115. Epub 2010/09/03. doi: 10.1007/978-1-60761-789-1_7 20809306.
69. Rust MJ, Bates M, Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods. 2006;3(10):793–5. Epub 2006/08/10. doi: 10.1038/nmeth929 16896339
70. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772
71. Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, et al. A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol. 2012;198(2):165–72. doi: 10.1083/jcb.201204085 22826121
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 9
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Raději si zajděte na oční! Jak souvisí citlivost zraku s rozvojem demence?
- Co způsobuje pooperační infekce? Na vině může být i naše vlastní mikrobiota
- Čeká nás průlom v diagnostice karcinomu pankreatu?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
Nejčtenější v tomto čísle
- Alleviating chronic ER stress by p38-Ire1-Xbp1 pathway and insulin-associated autophagy in C. elegans neurons
- Cocoonase is indispensable for Lepidoptera insects breaking the sealed cocoon
- A mega-analysis of expression quantitative trait loci in retinal tissue
- Adiponectin GWAS loci harboring extensive allelic heterogeneity exhibit distinct molecular consequences