#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The HEI10 Is a New ZMM Protein Related to Zip3


In numerous species, the formation of meiotic crossovers is largely under the control of a group of proteins known as ZMM. Here, we identified a new ZMM protein, HEI10, a RING finger-containing protein that is well conserved among species. We show that HEI10 is structurally and functionally related to the yeast Zip3 ZMM and that it is absolutely required for class I crossover (CO) formation in Arabidopsis thaliana. Furthermore, we show that it is present as numerous foci on the chromosome axes and the synaptonemal complex central element until pachytene. Then, from pachytene to diakinesis, HEI10 is retained at a limited number of sites that correspond to class I COs, where it co-localises with MLH1. Assuming that HEI10 early staining represents an early selection of recombination intermediates to be channelled into the ZMM pathway, HEI10 would therefore draw a continuity between early chosen recombination intermediates and final class I COs.


Vyšlo v časopise: The HEI10 Is a New ZMM Protein Related to Zip3. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002799
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002799

Souhrn

In numerous species, the formation of meiotic crossovers is largely under the control of a group of proteins known as ZMM. Here, we identified a new ZMM protein, HEI10, a RING finger-containing protein that is well conserved among species. We show that HEI10 is structurally and functionally related to the yeast Zip3 ZMM and that it is absolutely required for class I crossover (CO) formation in Arabidopsis thaliana. Furthermore, we show that it is present as numerous foci on the chromosome axes and the synaptonemal complex central element until pachytene. Then, from pachytene to diakinesis, HEI10 is retained at a limited number of sites that correspond to class I COs, where it co-localises with MLH1. Assuming that HEI10 early staining represents an early selection of recombination intermediates to be channelled into the ZMM pathway, HEI10 would therefore draw a continuity between early chosen recombination intermediates and final class I COs.


Zdroje

1. KeeneySGirouxCNKlecknerN 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 375 384

2. BishopDKZicklerD 2004 Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117 9 15

3. MullerHJ 1916 The mechanisms of crossing-over. American Naturalist 50 193 221

4. WhitbyMC 2005 Making crossovers during meiosis. Biochem Soc Trans 33 1451 1455

5. OsmanKHigginsJDSanchez-MoranEArmstrongSJFranklinFC 2011 Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190 523 544

6. BerchowitzLEFrancisKEBeyALCopenhaverGP 2007 The Role of AtMUS81 in Interference-Insensitive Crossovers in A. thaliana. PLoS Genet 3 e132 doi:10.1371/journal.pgen.0030132

7. De Los SantosTHunterNLeeCLarkinBLoidlJ 2003 The mus81/mms4 endonuclease acts independently of double-holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164 81 94

8. HigginsJDBucklingEFFranklinFCJonesGH 2008 Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54 152 162

9. LynnASoucekRBornerGV 2007 ZMM proteins during meiosis: Crossover artists at work. Chromosome Res 15 591 605

10. HigginsJDArmstrongSJFranklinFCJonesGH 2004 The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18 2557 2570

11. HigginsJDVignardJMercierRPughAGFranklinFC 2008 AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55 28 39

12. KneitzBCohenPEAvdievichEZhuLKaneMF 2000 MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14 1085 1097

13. Santucci-DarmaninSWalpitaDLespinasseFDesnuelleCAshleyT 2000 MSH4 acts in conjunction with MLH1 during mammalian meiosis. Faseb J 14 1539 1547

14. de BoerEStamPDietrichAJPastinkAHeytingC 2006 Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 103 9607 9612

15. MoensPBKolasNKTarsounasMMarconECohenPE 2002 The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J Cell Sci 115 1611 1622

16. NeytonSLespinasseFMoensPBPaulRGaudrayP 2004 Association between MSH4 (MutS homologue 4) and the DNA strand-exchange RAD51 and DMC1 proteins during mammalian meiosis. Mol Hum Reprod 10 917 924

17. BakerSMPlugAWProllaTABronnerCEHarrisAC 1996 Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13 336 342

18. HunterNBortsRH 1997 Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11 1573 1582

19. JacksonNSanchez-MoranEBucklingEArmstrongSJJonesGH 2006 Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. Embo J 25 1315 1323

20. KolasNKSvetlanovALenziMLMacalusoFPLipkinSM 2005 Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J Cell Biol 171 447 458

21. LipkinSMMoensPBWangVLenziMShanmugarajahD 2002 Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31 385 390

22. PageSLHawleyRS 2004 The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20 525 558

23. de BoerEHeytingC 2006 The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115 220 234

24. AgarwalSRoederGS 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102 245 255

25. ChuaPRRoederGS 1998 Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93 349 359

26. TsubouchiTZhaoHRoederGS 2006 The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev Cell 10 809 819

27. ShinoharaMOhSDHunterNShinoharaA 2008 Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40 299 309

28. de VriesSSBaartEBDekkerMSiezenAde RooijDG 1999 Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev 13 523 531

29. ChenCZhangWTimofejevaLGerardinYMaH 2005 The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J 43 321 334

30. MercierRJolivetSVezonDHuppeEChelyshevaL 2005 Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15 692 701

31. WangKTangDWangMLuJYuH 2009 MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122 2055 2063

32. ChelyshevaLGendrotGVezonDDoutriauxMPMercierR 2007 Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3 e83 doi:10.1371/journal.pgen.0030083

33. MazinaOMMazinAVNakagawaTKolodnerRDKowalczykowskiSC 2004 Saccharomyces cerevisiae Mer3 helicase stimulates 3′-5′ heteroduplex extension by Rad51; implications for crossover control in meiotic recombination. Cell 117 47 56

34. SnowdenTAcharyaSButzCBerardiniMFishelR 2004 hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15 437 451

35. MacaisneNVignardJMercierR 2011 SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J Cell Sci 124 2687 2691

36. MacaisneNNovatchkovaMPeireraLVezonDJolivetS 2008 SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr Biol 18 1432 1437

37. PerryJKlecknerNBornerGV 2005 Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102 17594 17599

38. ChengCHLoYHLiangSSTiSCLinFM 2006 SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20 2067 2081

39. WardJOReinholdtLGMotleyWWNiswanderLMDeaconDC 2007 Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 3 e139 doi:10.1371/journal.pgen.0030139

40. RossKJFranszPJonesGH 1996 A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4 507 516

41. Sanchez MoranEArmstrongSJSantosJLFranklinFCJonesGH 2001 Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res 9 121 128

42. BerchowitzLECopenhaverGP 2008 Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3 41 50

43. PerkinsDD 1949 Biochemical mutants in the smut fungus Ustilago maydis. Genetics 34 607 626

44. LiWChenCMarkmann-MulischUTimofejevaLSchmelzerE 2004 The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A

45. ArmstrongSJCarylAPJonesGHFranklinFC 2002 Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115 3645 3655

46. LhuissierFGOffenbergHHWittichPEVischerNOHeytingC 2007 The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19 862 876

47. ChelyshevaLGrandontLVrielynckNle GuinSMercierR 2010 An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res 129 143 153

48. HigginsJDSanchez-MoranEArmstrongSJJonesGHFranklinFC 2005 The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19 2488 2500

49. PuntaMCoggillPCEberhardtRYMistryJTateJ 2012 The Pfam protein families database. Nucleic acids research 40 D290 301

50. DelorenziMSpeedT 2002 An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18 617 625

51. AltenhoffAMDessimozC 2009 Phylogenetic and functional assessment of orthologs inference projects and methods. PLoS Comput Biol 5 e1000262 doi:10.1371/journal.pcbi.1000262

52. SayersEWBarrettTBensonDABoltonEBryantSH 2012 Database resources of the National Center for Biotechnology Information. Nucleic acids research 40 D13 25

53. MiHDongQMuruganujanAGaudetPLewisS 2010 PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic acids research 38 D204 210

54. WijeratneAJChenCZhangWTimofejevaLMaH 2006 The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol Biol Cell 17 1331 1343

55. SinghMKNicolasEGherrabyWDadkeDLessinS 2007 HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26 4825 4832

56. TobyGGGherrabyWColemanTRGolemisEA 2003 A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 23 2109 2122

57. SmithAPWeeraratnaATSpearsJRMeltzerPSBeckerD 2004 SAGE identification and fluorescence imaging analysis of genes and transcripts in melanomas and precursor lesions. Cancer Biol Ther 3 104 109

58. EdelmannWCohenPEKaneMLauKMorrowB 1996 Meiotic pachytene arrest in MLH1-deficient mice. Cell 85 1125 1134

59. WoodsLMHodgesCABaartEBakerSMLiskayM 1999 Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J Cell Biol 145 1395 1406

60. EdelmannWCohenPEKneitzBWinandNLiaM 1999 Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet 21 123 127

61. StrongERSchimentiJC 2010 Evidence Implicating CCNB1IP1, a RING Domain-Containing Protein Required for Meiotic Crossing Over in Mice, as an E3 SUMO Ligase. Genes (Basel) 1 440 451

62. BaudatFde MassyB 2007 Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15 565 577

63. De MuytAMercierRMezardCGrelonM 2009 Meiotic recombination and crossovers in plants. Genome Dyn 5 14 25

64. MoensPBChenDJShenZKolasNTarsounasM 1997 Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106 207 215

65. OsmanKSanchez-MoranEMannSCJonesGHFranklinFC 2009 Replication protein A (AtRPA1a) is required for class I crossover formation but is dispensable for meiotic DNA break repair. Embo J 28 394 404

66. StorlazziAGarganoSRuprich-RobertGFalqueMDavidM 2010 Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141 94 106

67. BhallaNWynneDJJantschVDernburgAF 2008 ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4 e1000235 doi:10.1371/journal.pgen.1000235

68. TsubouchiTMacqueenAJRoederGS 2008 Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22 3217 3226

69. GrelonMVezonDGendrotGPelletierG 2001 AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20 589 600

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

71. KongAThorleifssonGStefanssonHMassonGHelgasonA 2008 Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319 1398 1401

72. CarpenterAT 1975 Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule–a recombination-associated structure at pachytene? Proc Natl Acad Sci U S A 72 3186 3189

73. ZicklerDKlecknerN 1999 Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33 603 754

74. AndersonLKStackSM 2005 Recombination nodules in plants. Cytogenet Genome Res 109 198 204

75. GuillonHde MassyB 2002 An initiation site for meiotic crossing-over and gene conversion in the mouse. Nat Genet 32 296 299

76. PadmoreRCaoLKlecknerN 1991 Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66 1239 1256

77. ZicklerD 1977 Development of the synaptonemal complex and the “recombination nodules” during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw. Chromosoma 61 289 316

78. GilliesCB 1979 The Relationship between Synaptinemal Complexes, Recombination Nodules and Crossing over in NEUROSPORA CRASSA Bivalents and Translocation Quadrivalents. Genetics 91 1 17

79. LeflonMGrandontLEberFHuteauVCoritonO 2010 Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 22 2253 2264

80. BechtoldNEllisJPelletierG 1993 In Planta, Agrobacterium mediated gene transfer by integration of adult Arabidopsis thaliana plants. C R Acad Sci Paris 316 1194 1199

81. AlonsoJMStepanovaANLeisseTJKimCJChenH 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657

82. De MuytAPereiraLVezonDChelyshevaLGendrotG 2009 A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5 e1000654 doi:10.1371/journal.pgen.1000654

83. De MuytAVezonDGendrotGGalloisJLStevensR 2007 AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. Embo J

84. MoffattBAMcWhinnieEAAgarwalSKSchaffDA 1994 The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. Gene 143 211 216

85. ChelyshevaLDialloSVezonDGendrotGVrielynckN 2005 AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118 4621 4632

86. SmootMEOnoKRuscheinskiJWangPLIdekerT 2011 Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27 431 432

87. EdgarRC 2004 MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5 113

88. JantschVPasierbekPMuellerMMSchweizerDJantschM 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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#