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The Dissection of Meiotic Chromosome Movement in Mice Using an Electroporation Technique
Meiosis is a special type of cell division for gametogenesis, errors in which cause several genetic disorders such as infertility and Down syndrome. In meiotic prophase I, chromosomes are tethered to the nuclear envelope (NE) through telomeres, and move rapidly along the NE to get homologs aligned and juxtaposed. Following homologous recombination and synapsis, the bivalent chromosome structure is established, which promotes genetic varieties, and also ensures accurate chromosome segregation in following anaphase I. Although there have been extensive studies addressing meiotic chromosome dynamics in yeast and worms, the same in mammalian meiosis remains largely elusive. Here, we utilized an in vivo electroporation (EP) technique to visualize chromosome movement in live mouse spermatocytes. We, for the first time, define the meiotic sub-stages in live cells based on telomeres and chromosome axis morphologies, and reveal chromosome movements regulated in a stage-specific manner. Putting the live-observations together with our cytological observations in fixed cells, we propose that meiotic chromosome movements in mammals are mediated by the rail-tracking movement of telomeres along the MT cables surrounding the meiotic nucleus.
Vyšlo v časopise: The Dissection of Meiotic Chromosome Movement in Mice Using an Electroporation Technique. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004821
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004821Souhrn
Meiosis is a special type of cell division for gametogenesis, errors in which cause several genetic disorders such as infertility and Down syndrome. In meiotic prophase I, chromosomes are tethered to the nuclear envelope (NE) through telomeres, and move rapidly along the NE to get homologs aligned and juxtaposed. Following homologous recombination and synapsis, the bivalent chromosome structure is established, which promotes genetic varieties, and also ensures accurate chromosome segregation in following anaphase I. Although there have been extensive studies addressing meiotic chromosome dynamics in yeast and worms, the same in mammalian meiosis remains largely elusive. Here, we utilized an in vivo electroporation (EP) technique to visualize chromosome movement in live mouse spermatocytes. We, for the first time, define the meiotic sub-stages in live cells based on telomeres and chromosome axis morphologies, and reveal chromosome movements regulated in a stage-specific manner. Putting the live-observations together with our cytological observations in fixed cells, we propose that meiotic chromosome movements in mammals are mediated by the rail-tracking movement of telomeres along the MT cables surrounding the meiotic nucleus.
Zdroje
1. HiraokaY, DernburgAF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17 : 598–605.
2. KoszulR, KlecknerN (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19 : 716–724.
3. ChikashigeY, TsutsumiC, YamaneM, OkamasaK, HaraguchiT, et al. (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125 : 59–69.
4. WanatJJ, KimKP, KoszulR, ZandersS, WeinerB, et al. (2008) Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 4: e1000188.
5. Trelles-StickenE, AdelfalkC, LoidlJ, ScherthanH (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170 : 213–223.
6. ConradMN, LeeCY, ChaoG, ShinoharaM, KosakaH, et al. (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133 : 1175–1187.
7. JosephI, JiaD, LustigAJ (2005) Ndj1p-dependent epigenetic resetting of telomere size in yeast meiosis. Curr Biol 15 : 231–237.
8. KosakaH, ShinoharaM, ShinoharaA (2008) Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 4: e1000196.
9. PenknerA, TangL, NovatchkovaM, LadurnerM, FridkinA, et al. (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12 : 873–885.
10. PenknerAM, FridkinA, GloggnitzerJ, BaudrimontA, MachacekT, et al. (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139 : 920–933.
11. BaudrimontA, PenknerA, WoglarA, MachacekT, WegrostekC, et al. (2010) Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 6: e1001219.
12. WynneDJ, RogO, CarltonPM, DernburgAF (2012) Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 196 : 47–64.
13. SatoA, IsaacB, PhillipsCM, RilloR, CarltonPM, et al. (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139 : 907–919.
14. YaoKT, EllingsonDJ (1969) Observations on nuclear rotation and oscillation in Chinese hamster germinal cells in vitro. Exp Cell Res 55 : 39–42.
15. EllingsonDJ, YaoKT (1970) Growth and observations of Chinese hamster seminiferous epithelium in vitro. J Cell Sci 6 : 195–205.
16. ParvinenM, SoderstromKO (1976) Chromosome rotation and formation of synapsis. Nature 260 : 534–535.
17. DingX, XuR, YuJ, XuT, ZhuangY, et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12 : 863–872.
18. MorimotoA, ShibuyaH, ZhuX, KimJ, IshiguroK, et al. (2012) A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 198 : 165–172.
19. ShibuyaH, IshiguroK, WatanabeY (2014) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16 : 145–156.
20. ShibuyaH, WatanabeY (2014) The meiosis-specific modification of mammalian telomeres. Cell Cycle 13 : 2024–8.
21. SchrammS, FrauneJ, NaumannR, Hernandez-HernandezA, HoogC, et al. (2011) A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet 7: e1002088.
22. GoshimaG, KiyomitsuT, YodaK, YanagidaM (2003) Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol 160 : 25–39.
23. PolakovaS, CipakL, GreganJ (2011) RAD21L is a novel kleisin subunit of the cohesin complex. Cell Cycle 10 : 1892–1893.
24. LeeJ, HiranoT (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192 : 263–276.
25. HerranY, Gutierrez-CaballeroC, Sanchez-MartinM, HernandezT, VieraA, et al. (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30 : 3091–3105.
26. Gutierrez-CaballeroC, HerranY, Sanchez-MartinM, SujaJA, BarberoJL, et al. (2011) Identification and molecular characterization of the mammalian alpha-kleisin RAD21L. Cell Cycle 10 : 1477–1487.
27. YuanL, LiuJG, ZhaoJ, BrundellE, DaneholtB, et al. (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 5 : 73–83.
28. HornHF, KimDI, WrightGD, WongES, StewartCL, et al. (2013) A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 202 : 1023–1039.
29. IshiguroK, KimJ, ShibuyaH, Hernandez-HernandezA, SuzukiA, et al. (2014) Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes. Genes Dev 28 : 594–607.
30. SalonenK, ParankoJ, ParvinenM (1982) A colcemid-sensitive mechanism involved in regulation of chromosome movements during meiotic pairing. Chromosoma 85 : 611–618.
31. DingDQ, ChikashigeY, HaraguchiT, HiraokaY (1998) Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J Cell Sci 111 (Pt 6) 701–712.
32. CowanCR, CandeWZ (2002) Meiotic telomere clustering is inhibited by colchicine but does not require cytoplasmic microtubules. J Cell Sci 115 : 3747–3756.
33. KoszulR, KimKP, PrentissM, KlecknerN, KameokaS (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133 : 1188–1201.
34. QiaoH, ChenJK, ReynoldsA, HoogC, PaddyM, et al. (2012) Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLoS Genet 8: e1002790.
35. BisigCG, GuiraldelliMF, KouznetsovaA, ScherthanH, HoogC, et al. (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8: e1002701.
36. HarperL, GolubovskayaI, CandeWZ (2004) A bouquet of chromosomes. J Cell Sci 117 : 4025–4032.
37. ScherthanH (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2 : 621–627.
38. von WettsteinD (1984) The synaptonemal complex and genetic segregation. Symp Soc Exp Biol 38 : 195–231.
39. ZicklerD, KlecknerN (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32 : 619–697.
40. ZicklerD (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115 : 158–174.
41. McKeeBD (2004) Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim Biophys Acta 1677 : 165–180.
42. Trelles-StickenE, DresserME, ScherthanH (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151 : 95–106.
43. MosesMJ (1969) Structure and function of the synaptonemal complex. Genetics 61: Suppl: 41–51.
44. SatoT, KatagiriK, GohbaraA, InoueK, OgonukiN, et al. (2011) In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471 : 504–507.
45. SatoT, KatagiriK, KubotaY, OgawaT (2013) In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc 8 : 2098–2104.
46. SaitoT (2006) In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc 1 : 1552–1558.
47. MatsudaT, CepkoCL (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 101 : 16–22.
48. ShojiM, ChumaS, YoshidaK, MoritaT, NakatsujiN (2005) RNA interference during spermatogenesis in mice. Dev Biol 282 : 524–534.
49. ScherthanH, WangH, AdelfalkC, WhiteEJ, CowanC, et al. (2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 : 16934–16939.
50. YoshidaM, KatsuyamaS, TatehoK, NakamuraH, MiyoshiJ, et al. (2013) Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J Cell Biol 200 : 385–395.
51. LiebeB, AlsheimerM, HoogC, BenaventeR, ScherthanH (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol Biol Cell 15 : 827–837.
52. CarltonPM, CowanCR, CandeWZ (2003) Directed motion of telomeres in the formation of the meiotic bouquet revealed by time course and simulation analysis. Mol Biol Cell 14 : 2832–2843.
53. BassHW, MarshallWF, SedatJW, AgardDA, CandeWZ (1997) Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol 137 : 5–18.
54. VantardM, LevilliersN, HillAM, AdoutteA, LambertAM (1990) Incorporation of Paramecium axonemal tubulin into higher plant cells reveals functional sites of microtubule assembly. Proc Natl Acad Sci U S A 87 : 8825–8829.
55. CowanCR, CarltonPM, CandeWZ (2002) Reorganization and polarization of the meiotic bouquet-stage cell can be uncoupled from telomere clustering. J Cell Sci 115 : 3757–3766.
56. PetersAH, PlugAW, van VugtMJ, de BoerP (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5 : 66–68.
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