Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in

English version České info

The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2–dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

Vyšlo v časopise: Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in. PLoS Genet 6(11): e32767. doi:10.1371/journal.pgen.1001219
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001219

Souhrn

Zdroje

1. PetronczkiM

SiomosM

NasmythK

2003 Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112 423 440

2. ScherthanH

2001 A bouquet makes ends meet. Nat Rev Mol Cell Biol 2 621 627

3. ChikashigeY

HaraguchiT

HiraokaY

2007 Another way to move chromosomes. Chromosoma 116 497 505

4. FridkinA

PenknerA

JantschV

GruenbaumY

2008 SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 66 1518 1533

5. HiraokaY

DernburgAF

2009 The SUN rises on meiotic chromosome dynamics. Dev Cell 17 598 605

6. ConradMN

LeeCY

ChaoG

ShinoharaM

KosakaH

2008 Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133 1175 1187

7. 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

8. ChikashigeY

TsutsumiC

YamaneM

OkamasaK

HaraguchiT

2006 Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125 59 69

9. SheehanM

PawlowskiW

2009 Live imaging of rapid chromosome movements in meiotic prophase I in maize. Proc Natl Acad Sci USA 106 20989 20994

10. ScherthanH

WangH

AdelfalkC

WhiteEJ

CowanC

2007 Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 16934 16939

11. 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

12. WanatJJ

KimKP

KoszulR

ZandersS

WeinerB

2008 Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 4 e1000188 doi:10.1371/journal.pgen.1000188

13. KosakaH

ShinoharaM

ShinoharaA

2008 Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet 4 e1000196 doi:10.1371/journal.pgen.1000196

14. ConradMN

LeeCY

WilkersonJL

DresserME

2007 MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 8863 8868

15. ConradMN

DominguezAM

DresserME

1997 Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276 1252 1255

16. WuHY

BurgessSM

2006 Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16 2473 2479

17. DernburgAF

McDonaldK

MoulderG

BarsteadR

DresserM

1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94 387 398

18. ColaiacovoMP

2006 The many facets of SC function during C. elegans meiosis. Chromosoma 115 195 211

19. SmolikovS

Schild-PrüfertK

ColaiácovoMP

2009 A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet 5 e1000669 doi:10.1371/journal.pgen.1000669

20. CouteauF

ZetkaM

2005 HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19 2744 2756

21. Martinez-PerezE

VilleneuveAM

2005 HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19 2727 2743

22. McKimKS

HowellAM

RoseAM

1988 The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics 120 987 1001

23. RosenbluthRE

BaillieDL

1981 The genetic analysis of a reciprocal translocation, eT1(III; V), in Caenorhabditis elegans. Genetics 99 415 428

24. MacQueenAJ

PhillipsCM

BhallaN

WeiserP

VilleneuveAM

2005 Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123 1037 1050

25. PhillipsCM

WongC

BhallaN

CarltonPM

WeiserP

2005 HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123 1051 1063

26. PhillipsCM

DernburgAF

2006 A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans. Dev Cell 11 817 829

27. PhillipsC

MengX

ZhangL

ChretienJ

UrnovF

2009 Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat Cell Biol 11 934 942

28. PenknerA

FridkinA

GloggnitzerJ

BaudrimontA

MachacekT

2009 Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1. Cell 139 920 933

29. SatoA

IsaacB

PhillipsC

RilloR

CarltonP

2009 Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis. Cell 139 907 919

30. PenknerA

TangL

NovatchkovaM

LadurnerM

FridkinA

2007 The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12 873 885

31. MacQueenA

VilleneuveA

2001 Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15 1674 1687

32. JantschV

TangL

PasierbekP

PenknerA

NayakS

2007 Caenorhabditis elegans prom-1 is required for meiotic prophase progression and homologous chromosome pairing. Mol Biol Cell 18 4911 4920

33. TangL

MachacekT

MamnunYM

PenknerA

GloggnitzerJ

2010 Mutations in C. elegans him-19 show meiotic defects that worsen with age. MBC 21 885 896

34. SmolikovS

Schild-PrüfertK

ColaiácovoMP

2008 CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis. PLoS Genet 4 e1000088 doi:10.1371/journal.pgen.1000088

35. HubbardEJA

GreensteinD

2005 Introduction to the germ line. WormBook the online review of C elegans biology 1 4

36. MaloneCJ

MisnerL

Le BotN

TsaiMC

CampbellJM

2003 The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115 825 836

37. MacQueenAJ

ColaiácovoMP

McDonaldK

VilleneuveAM

2002 Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16 2428 2442

38. ColaiácovoMP

MacQueenAJ

Martinez-PerezE

McDonaldK

AdamoA

2003 Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5 463 474

39. SmolikovS

EizingerA

HurlburtA

RogersE

VilleneuveAM

2007 Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 176 2027 2033

40. CouteauF

NabeshimaK

VilleneuveA

ZetkaM

2004 A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14 585 592

41. SchmittJ

BenaventeR

HodzicD

HoogC

StewartCL

2007 Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci U S A 104 7426 7431

42. StorlazziA

GarganoS

Ruprich-RobertG

FalqueM

DavidM

2010 Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141 94 106

43. CarltonPM

FarruggioAP

DernburgAF

2006 A link between meiotic prophase progression and crossover control. PLoS Genet 2 e12 doi:10.1371/journal.pgen.0020012

44. BrennerS

1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

45. HayashiM

ChinGM

VilleneuveAM

2007 C. elegans Germ Cells Switch between Distinct Modes of Double-Strand Break Repair During Meiotic Prophase Progression. PLoS Genet 3 e191 doi:10.1371/journal.pgen.0030191

46. JantschV

PasierbekP

MuellerMM

SchweizerD

JantschM

2004 Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24 7998 8006