The Chromosome Axis Mediates Feedback Control of CHK-2 to Ensure Crossover Formation in C. elegans

Developmental Cell

Volumn 35, Issue 2, 2015, Pages 247-261

  Kim, Yumi ^a,b   Kostow, Nora ^a,b   Dernburg, Abby F ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; POLO LIKE KINASE 2; ZINC FINGER PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CHK-2 PROTEIN, C ELEGANS; POLO-LIKE KINASE 2, C ELEGANS; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CROSSING OVER; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FEEDBACK SYSTEM; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CHROMOSOME; GENETICS; METABOLISM;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHECKPOINT KINASE 2; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOMES; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; MEIOSIS; PROTEIN-SERINE-THREONINE KINASES;

EID: 84945135696     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.09.021     Document Type: Article

References (64)

1. Aravind L., Koonin E.V. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem. Sci. 1998, 23:284-286.
2. Bailis J.M., Roeder G.S. Pachytene exit controlled by reversal of Mek1-dependent phosphorylation. Cell 2000, 101:211-221.
3. Bhalla N., Wynne D.J., Jantsch V., Dernburg A.F. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet. 2008, 4:e1000235.
4. Bishop D.K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 1992, 69:439-456.
5. Börner G.V., Barot A., Kleckner N. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc. Natl. Acad. Sci. USA 2008, 105:3327-3332.
6. Carballo J.A., Johnson A.L., Sedgwick S.G., Cha R.S. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 2008, 132:758-770.
7. Colaiácovo M.P., MacQueen A.J., Martinez-Perez E., McDonald K., Adamo A., La Volpe A., Villeneuve A.M. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 2003, 5:463-474.
8. Collin P., Nashchekina O., Walker R., Pines J. The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat. Cell Biol. 2013, 15:1378-1385.
9. Couteau F., Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005, 19:2744-2756.
10. Daniel K., Lange J., Hached K., Fu J., Anastassiadis K., Roig I., Cooke H.J., Stewart A.F., Wassmann K., Jasin M., et al. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat. Cell Biol. 2011, 13:599-610.
11. De Antoni A., Pearson C.G., Cimini D., Canman J.C., Sala V., Nezi L., Mapelli M., Sironi L., Faretta M., Salmon E.D., Musacchio A. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 2005, 15:214-225.
12. Dernburg A.F., McDonald K., Moulder G., Barstead R., Dresser M., Villeneuve A.M. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 1998, 94:387-398.
13. Dick A.E., Gerlich D.W. Kinetic framework of spindle assembly checkpoint signalling. Nat. Cell Biol. 2013, 15:1370-1377.
14. Dickinson D.J., Ward J.D., Reiner D.J., Goldstein B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 2013, 10:1028-1034.
15. Edelmann W., Cohen P.E., Kane M., Lau K., Morrow B., Bennett S., Umar A., Kunkel T., Cattoretti G., Chaganti R., et al. Meiotic pachytene arrest in MLH1-deficient mice. Cell 1996, 85:1125-1134.
16. Elia A.E.H., Cantley L.C., Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 2003, 299:1228-1231.
17. Frøkjaer-Jensen C., Davis M.W., Hopkins C.E., Newman B.J., Thummel J.M., Olesen S.P., Grunnet M., Jorgensen E.M. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 2008, 40:1375-1383.
18. Ghabrial A., Schüpbach T. Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat. Cell Biol. 1999, 1:354-357.
19. Goodyer W., Kaitna S., Couteau F., Ward J.D., Boulton S.J., Zetka M. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 2008, 14:263-274.
20. Harper N.C., Rillo R., Jover-Gil S., Assaf Z.J., Bhalla N., Dernburg A.F. Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev. Cell 2011, 21:934-947.
21. Hartwell L.H., Weinert T.A. Checkpoints: controls that ensure the order of cell cycle events. Science 1989, 246:629-634.
22. Higashitani A., Aoki H., Mori A., Sasagawa Y., Takanami T., Takahashi H. Caenorhabditis elegans Chk2-like gene is essential for meiosis but dispensable for DNA repair. FEBS Lett. 2000, 485:35-39.
23. Joshi N., Barot A., Jamison C., Börner G.V. Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet. 2009, 5:e1000557.
24. Kelly K.O., Dernburg A.F., Stanfield G.M., Villeneuve A.M. Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 2000, 156:617-630.
25. Kim Y., Rosenberg S.C., Kugel C.L., Kostow N., Rog O., Davydov V., Su T.Y., Dernburg A.F., Corbett K.D. The chromosome axis controls meiotic events through a hierarchical assembly of HORMA domain proteins. Dev. Cell 2014, 31:487-502.
26. Labella S., Woglar A., Jantsch V., Zetka M. Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev. Cell 2011, 21:948-958.
27. Li J., Williams B.L., Haire L.F., Goldberg M., Wilker E., Durocher D., Yaffe M.B., Jackson S.P., Smerdon S.J. Structural and functional versatility of the FHA domain in DNA-damage signaling by the tumor suppressor kinase Chk2. Mol. Cell 2002, 9:1045-1054.
28. London N., Biggins S. Signalling dynamics in the spindle checkpoint response. Nat. Rev. Mol. Cell Biol. 2014, 15:736-747.
29. Luo X., Tang Z., Xia G., Wassmann K., Matsumoto T., Rizo J., Yu H. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 2004, 11:338-345.
30. Lydall D., Nikolsky Y., Bishop D.K., Weinert T. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 1996, 383:840-843.
31. MacQueen A.J., Hochwagen A. Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol. 2011, 21:393-400.
32. MacQueen A.J., Villeneuve A.M. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 2001, 15:1674-1687.
33. MacQueen A.J., Colaiácovo M.P., McDonald K., Villeneuve A.M. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002, 16:2428-2442.
34. Mapelli M., Massimiliano L., Santaguida S., Musacchio A. The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell 2007, 131:730-743.
35. Martinez-Perez E., Villeneuve A.M. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005, 19:2727-2743.
36. Martinez-Perez E., Schvarzstein M., Barroso C., Lightfoot J., Dernburg A.F., Villeneuve A.M. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 2008, 22:2886-2901.
37. Matsuoka S., Huang M., Elledge S.J. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998, 282:1893-1897.
38. Meneely P.M., McGovern O.L., Heinis F.I., Yanowitz J.L. Crossover distribution and frequency are regulated by him-5 in Caenorhabditis elegans. Genetics 2012, 190:1251-1266.
39. Nabeshima K., Villeneuve A.M., Hillers K.J. Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 2004, 168:1275-1292.
40. Niu H., Wan L., Baumgartner B., Schaefer D., Loidl J., Hollingsworth N.M. Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol. Biol. Cell 2005, 16:5804-5818.
41. Niu H., Li X., Job E., Park C., Moazed D., Gygi S.P., Hollingsworth N.M. Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol. Cell. Biol. 2007, 27:5456-5467.
42. O'Neill T., Giarratani L., Chen P., Iyer L., Lee C.-H., Bobiak M., Kanai F., Zhou B.-B., Chung J.H., Rathbun G.A. Determination of substrate motifs for human Chk1 and hCds1/Chk2 by the oriented peptide library approach. J. Biol. Chem. 2002, 277:16102-16115.
43. Oishi I., Iwai K., Kagohashi Y., Fujimoto H., Kariya K., Kataoka T., Sawa H., Okano H., Otani H., Yamamura H., Minami Y. Critical role of Caenorhabditis elegans homologs of Cds1 (Chk2)-related kinases in meiotic recombination. Mol. Cell. Biol. 2001, 21:1329-1335.
44. Penkner A., Tang L., Novatchkova M., Ladurner M., Fridkin A., Gruenbaum Y., Schweizer D., Loidl J., Jantsch V. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev. Cell 2007, 12:873-885.
45. Penkner A.M., Fridkin A., Gloggnitzer J., Baudrimont A., Machacek T., Woglar A., Csaszar E., Pasierbek P., Ammerer G., Gruenbaum Y., Jantsch V. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 2009, 139:920-933.
46. Phillips C.M., Dernburg A.F. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 2006, 11:817-829.
47. Phillips C.M., Wong C., Bhalla N., Carlton P.M., Weiser P., Meneely P.M., Dernburg A.F. HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 2005, 123:1051-1063.
48. Phillips C.M., Meng X., Zhang L., Chretien J.H., Urnov F.D., Dernburg A.F. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat. Cell Biol. 2009, 11:934-942.
49. Pittman D.L., Cobb J., Schimenti K.J., Wilson L.A., Cooper D.M., Brignull E., Handel M.A., Schimenti J.C. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1998, 1:697-705.
50. Roeder G.S., Bailis J.M. The pachytene checkpoint. Trends Genet. 2000, 16:395-403.
51. Rog O., Dernburg A.F. Direct Visualization Reveals Kinetics of Meiotic Chromosome Synapsis. Cell Rep. 2015, 10:1639-1645.
52. Roig I., Dowdle J.A., Toth A., de Rooij D.G., Jasin M., Keeney S. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet. 2010, 6:e1001062.
53. Rosu S., Zawadzki K.A., Stamper E.L., Libuda D.E., Reese A.L., Dernburg A.F., Villeneuve A.M. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genet. 2013, 9:e1003674.
54. Sato A., Isaac B., Phillips C.M., Rillo R., Carlton P.M., Wynne D.J., Kasad R.A., Dernburg A.F. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 2009, 139:907-919.
55. Shin Y.-H., Choi Y., Erdin S.U., Yatsenko S.A., Kloc M., Yang F., Wang P.J., Meistrich M.L., Rajkovic A. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet. 2010, 6:e1001190.
56. Silva N., Ferrandiz N., Barroso C., Tognetti S., Lightfoot J., Telecan O., Encheva V., Faull P., Hanni S., Furger A., et al. The fidelity of synaptonemal complex assembly is regulated by a signaling mechanism that controls early meiotic progression. Dev. Cell 2014, 31:503-511.
57. Stamper E.L., Rodenbusch S.E., Rosu S., Ahringer J., Villeneuve A.M., Dernburg A.F. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 2013, 9:e1003679.
58. Subramanian V.V., Hochwagen A. The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb. Perspect. Biol. 2014, 6:a016675.
59. Woglar A., Daryabeigi A., Adamo A., Habacher C., Machacek T., La Volpe A., Jantsch V. Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet. 2013, 9:e1003335.
60. Wojtasz L., Daniel K., Roig I., Bolcun-Filas E., Xu H., Boonsanay V., Eckmann C.R., Cooke H.J., Jasin M., Keeney S., 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:e1000702.
61. Wojtasz L., Cloutier J.M., Baumann M., Daniel K., Varga J., Fu J., Anastassiadis K., Stewart A.F., Reményi A., Turner J.M.A., Tóth A. Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev. 2012, 26:958-973.
62. Wynne D.J., Rog O., Carlton P.M., Dernburg A.F. Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J. Cell Biol. 2012, 196:47-64.
63. Xu L., Weiner B.M., Kleckner N. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 1997, 11:106-118.
64. Zetka M.C., Kawasaki I., Strome S., Müller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 1999, 13:2258-2270.