AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms
Sexually reproducing species produce offspring that are genetically unique from one another, despite having the same parents. This uniqueness is created by meiosis, which is a specialized cell division. After meiosis each parent transmits half of their DNA, but each time this occurs, the 'half portion' of DNA transmitted to offspring is different from the previous. The differences are due to resorting the parental chromosomes, but also recombining them. Here we describe a gene—FIDGETIN-LIKE 1—which limits the amount of recombination that occurs during meiosis. Previously we identified a gene with a similar function, FANCM. FIGL1 and FANCM operate through distinct mechanisms. This discovery will be useful to understand more, from an evolutionary perspective, why recombination is naturally limited. Also this has potentially significant applications for plant breeding which is largely about sampling many 'recombinants' to find individuals that have heritable advantages compared to their parents.
Vyšlo v časopise:
AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005369
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005369
Souhrn
Sexually reproducing species produce offspring that are genetically unique from one another, despite having the same parents. This uniqueness is created by meiosis, which is a specialized cell division. After meiosis each parent transmits half of their DNA, but each time this occurs, the 'half portion' of DNA transmitted to offspring is different from the previous. The differences are due to resorting the parental chromosomes, but also recombining them. Here we describe a gene—FIDGETIN-LIKE 1—which limits the amount of recombination that occurs during meiosis. Previously we identified a gene with a similar function, FANCM. FIGL1 and FANCM operate through distinct mechanisms. This discovery will be useful to understand more, from an evolutionary perspective, why recombination is naturally limited. Also this has potentially significant applications for plant breeding which is largely about sampling many 'recombinants' to find individuals that have heritable advantages compared to their parents.
Zdroje
1. Goldfarb T, Lichten M (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8: e1000520. doi: 10.1371/journal.pbio.1000520 20976044
2. Zickler D, Kleckner NE (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754. doi: 10.1146/annurev.genet.33.1.603 10690419
3. De Massy B (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet 47: 563–599. doi: 10.1146/annurev-genet-110711-155423 24050176
4. Whitby MC (2005) Making crossovers during meiosis. Biochem Soc Trans 33: 1451–1455. 16246144
5. Lao JP, Hunter N (2010) Trying to avoid your sister. PLoS Biol 8: e1000519. doi: 10.1371/journal.pbio.1000519 20976046
6. Cloud V, Chan Y-L, Grubb J, Budke B, Bishop DK (2012) Rad51 Is an accessory factor for Dmc1-Mediated joint molecule formation during meiosis. Science 337: 1222–1225. doi: 10.1126/science.1219379 22955832
7. Hong S, Sung Y, Yu M, Lee M, Kleckner N, et al. (2013) The logic and mechanism of homologous recombination partner choice. Mol Cell 51: 440–453. doi: 10.1016/j.molcel.2013.08.008 23973374
8. Kurzbauer M-T, Uanschou C, Chen D, Schlögelhofer P (2012) The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell 24: 2058–2070. doi: 10.1105/tpc.112.098459 22589466
9. Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D, et al. (2013) Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in Arabidopsis. Plant Cell 25: 4924–4940. doi: 10.1105/tpc.113.118521 24363313
10. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, et al. (2013) Meiotic recombination in Arabidopsis Is catalysed by DMC1, with RAD51 playing a supporting role. PLoS Genet 9. doi: 10.1371/journal.pgen.1003787
11. Humphryes N, Hochwagen A (2014) A non-sister act: Recombination template choice during meiosis. Exp Cell Res. doi: 10.1016/j.yexcr.2014.08.024
12. Azumi Y, Liu D, Zhao D, Li W, Wang G, et al. (2002) Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J 21: 3081–3095. doi: 10.1093/emboj/cdf285 12065421
13. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, et al. (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 19763177
14. Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47–57. 11461701
15. Hollingsworth NM, Brill SJ (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18: 117–125. doi: 10.1101/gad.1165904 14752007
16. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523–544. doi: 10.1111/j.1469-8137.2011.03665.x 21366595
17. Lynn A, Soucek R, Börner GV (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605. doi: 10.1007/s10577-007-1150-1 17674148
18. Zakharyevich K, Tang S, Ma Y, Hunter N (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334–347. doi: 10.1016/j.cell.2012.03.023 22500800
19. Berchowitz LE, Copenhaver GP (2010) Genetic interference: don’t stand so close to me. Curr Genomics 11: 91–102. doi: 10.2174/138920210790886835 20885817
20. Anderson LK, Lohmiller LD, Tang X, Hammond DB, Javernick L, et al. (2014) Combined fluorescent and electron microscopic imaging unveils the specific properties of two classes of meiotic crossovers. Proc Natl Acad Sci U S A. doi: 10.1073/pnas.1406846111
21. Higgins JD, Buckling EF, Franklin FCH, Jones GH (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. doi: 10.1111/j.1365-313X.2008.03403.x 18182028
22. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132. doi: 10.1371/journal.pgen.0030132 17696612
23. Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M (2014) The molecular biology of meiosis in plants. Annu Rev Plant Biol 66: 1–31. doi: 10.1146/annurev-arplant-050213-035923 25423078
24. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, et al. (2012) FANCM limits meiotic crossovers. Science 336: 1588–1590. doi: 10.1126/science.1220381 22723424
25. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, et al. (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254–1258. doi: 10.1126/science.1183112 20203049
26. Lorenz A, Osman F, Sun W, Nandi S, Steinacher R, et al. (2012) The fission yeast FANCM ortholog directs non-crossover recombination during meiosis. Science 336: 1585–1588. doi: 10.1126/science.1220111 22723423
27. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J, et al. (2012) BLM helicase ortholog Sgs1 Is a central regulator of meiotic recombination intermediate metabolism. Mol Cell 46: 43–53. doi: 10.1016/j.molcel.2012.02.020 22500736
28. Rockmill B, Fung JC, Branda SS, Roeder GS (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13: 1954–1962. doi: 10.1016/j.cub.2003.10.059 14614820
29. Tang S, Wu MKY, Zhang R, Hunter N (2015) Pervasive and essential roles of the Top3-Rmi1 decatenase orchestrate recombination and facilitate chromosome segregation in meiosis. Mol Cell 57: 607–621. doi: 10.1016/j.molcel.2015.01.021 25699709
30. Kaur H, De Muyt A, Lichten M (2015) Top3-Rmi1 DNA single-strand decatenase is integral to the formation and resolution of meiotic recombination intermediates. Mol Cell 57: 583–594. doi: 10.1016/j.molcel.2015.01.020 25699707
31. Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A, et al. (2014) FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res 42: 9087–9095. doi: 10.1093/nar/gku614 25038251
32. Yuan J, Chen J (2013) FIGNL1-containing protein complex is required for efficient homologous recombination repair. Proc Natl Acad Sci U S A 2013. doi: 10.1073/pnas.1220662110
33. L′Hôte D, Vatin M, Auer J, Castille J, Passet B, et al. (2011) Fidgetin-like1 is a strong candidate for a dynamic impairment of male meiosis leading to reduced testis weight in mice. PLoS One 6: e27582. doi: 10.1371/journal.pone.0027582 22110678
34. Wu L, Hickson ID (2003) The Bloom’s syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870–874. doi: 10.1038/nature02253 14685245
35. Berchowitz LE, Copenhaver GP (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3: 41–50. doi: 10.1038/nprot.2007.491 18193020
36. Ziolkowski PA, Berchowitz LE, Lambing C, Yelina NE, Zhao X, et al. (2015) Juxtaposition of heterozygosity and homozygosity during meiosis causes reciprocal crossover remodeling via interference. eLife 4. doi: 10.7554/eLife.03708
37. Rockmill B, Voelkel-Meiman K, Roeder GS (2006) Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174: 1745–1754. doi: 10.1534/genetics.106.058933 17028345
38. Ghosh S, Feingold E, Dey SK (2009) Etiology of Down syndrome: Evidence for consistent association among altered meiotic recombination, nondisjunction, and maternal age across populations. Am J Med Genet A 149A: 1415–1420. doi: 10.1002/ajmg.a.32932 19533770
39. Oliver TR, Feingold E, Yu K, Cheung V, Tinker S, et al. (2008) New insights into human nondisjunction of chromosome 21 in oocytes. PLoS Genet 4: e1000033. doi: 10.1371/journal.pgen.1000033 18369452
40. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, et al. (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. doi: 10.1159/000314096 20628250
41. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3,whereas the other one is not. Curr Biol 15: 692–701. doi: 10.1016/j.cub.2005.02.056 15854901
42. Drouaud J, Mercier R, Chelysheva L, Bérard A, Falque M, et al. (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3: e106. doi: 10.1371/journal.pgen.0030106 17604455
43. Giraut L, Falque M, Drouaud J, Pereira L, Martin OC, et al. (2011) Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet 7: e1002354. doi: 10.1371/journal.pgen.1002354 22072983
44. Mercier R, Grelon M (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120: 281–290. doi: 10.1159/000121077 18504357
45. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, et al. (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11: 1623–1634. doi: 10.1105/tpc.11.9.1623 10488231
46. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, et al. (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3: 1894–1906. doi: 10.1371/journal.pgen.0030176 17937504
47. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A 101: 10596–10601. doi: 10.1073/pnas.0404110101 15249667
48. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, et al. (2013) Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet 9: e1003978. doi: 10.1371/journal.pgen.1003978 24367271
49. Crismani W, Girard C, Mercier R (2013) Tinkering with meiosis. J Exp Bot 64: 55–65. doi: 10.1093/jxb/ers314 23136169
50. Henderson IR (2012) Control of meiotic recombination frequency in plant genomes. Curr Opin Plant Biol 15: 556–561. doi: 10.1016/j.pbi.2012.09.002 23017241
51. Wijnker E, de Jong H (2008) Managing meiotic recombination in plant breeding. Trends Plant Sci 13: 640–646. doi: 10.1016/j.tplants.2008.09.004 18948054
52. Evans E, Alani EE (2000) Roles for mismatch repair factors in regulating genetic recombination. Mol Cell Biol 20: 7839–7844. 11027255
53. Whitby MC (2010) The FANCM family of DNA helicases/translocases. DNA Repair 9: 224–236. doi: 10.1016/j.dnarep.2009.12.012 20117061
54. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3: e196. doi: 10.1371/journal.pbio.0030196 15907155
55. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, et al. (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419–423. doi: 10.1038/nature10414 21874022
56. Wijnker E, Velikkakam James G, Ding J, Becker F, Klasen JR, et al. (2013) The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2: e01426. doi: 10.7554/eLife.01426 24347547
57. Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S, et al. (2013) Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet 9: e1003922. doi: 10.1371/journal.pgen.1003922 24244190
58. Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N (2008) RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell 31: 324–336. doi: 10.1016/j.molcel.2008.07.006 18691965
59. Jessop L, Lichten M (2008) Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol Cell 31: 313–323. doi: 10.1016/j.molcel.2008.05.021 18691964
60. Oh SD, Lao JP, Hwang PY-H, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259–272. doi: 10.1016/j.cell.2007.05.035 17662941
61. Wan L, Han J, Liu T, Dong S, Xie F, et al. (2013) Scaffolding protein SPIDR/KIAA0146 connects the Bloom syndrome helicase with homologous recombination repair. Proc Natl Acad Sci U S A 110: 10646–10651. doi: 10.1073/pnas.1220921110 23509288
62. Séguéla-Arnaud M, Crismani W, Larchevêque C, Mazel J, Froger N, et al. (2015) Multiple mechanisms limit meiotic crossovers: TOP3α and two BLM homologs antagonize crossovers in parallel to FANCM. Proc Natl Acad Sci: 201423107. doi: 10.1073/pnas.1423107112
63. Beyer a (1997) Sequence analysis of the AAA protein family. Protein Sci 6: 2043–2058. doi: 10.1002/pro.5560061001 9336829
64. Frickey T, Lupas A (2004) Phylogenetic analysis of AAA proteins. J Struct Biol 146: 2–10. 15037233
65. Vale RD (2000) AAA proteins. Lords of the ring. J Cell Biol 150: F13–F19. 10893253
66. McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75: 419–429. 8221885
67. Chen C, Jomaa A, Ortega J, Alani EE (2014) Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A 111: E44–E53. doi: 10.1073/pnas.1310755111 24367111
68. Peng W, Lin Z, Li W, Lu J, Shen Y, et al. (2013) Structural insights into the unusually strong ATPase activity of the AAA domain of the Caenorhabditis elegans fidgetin-like 1 (FIGL-1) protein. J Biol Chem 288: 29305–29312. doi: 10.1074/jbc.M113.502559 23979136
69. Vajjhala PR, Wong JS, To H-Y, Munn AL (2006) The beta domain is required for Vps4p oligomerization into a functionally active ATPase. FEBS J 273: 2357–2373. doi: 10.1111/j.1742-4658.2006.05238.x 16704411
70. Lupas AN, Martin J (2002) AAA proteins. Curr Opin Struct Biol 12: 746–753. doi: 10.1016/S0959-440X(02)00388-3 12504679
71. Solinger J a, Kiianitsa K, Heyer WD (2002) Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell 10: 1175–1188. doi: 10.1016/S1097-2765(02)00743-8 12453424
72. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E, et al. (2012) Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet 8: e1002507. doi: 10.1371/journal.pgen.1002507 22319460
73. Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21: 2220–2233. doi: 10.1101/gad.439007 17785529
74. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, et al. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48: 206–216. doi: 10.1111/j.1365-313X.2006.02867.x 17018031
75. Pradillo M, Lõpez E, Linacero R, Romero C, Cuñado N, et al. (2012) Together yes, but not coupled: New insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J 69: 921–933. doi: 10.1111/j.1365-313X.2011.04845.x 22066484
76. Chelysheva L, Gendrot G, Vezon D, Doutriaux M- P, Mercier R, et al. (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 17530928
77. Macaisne N, Novatchkova M, Peirera L, Vezon D, Jolivet S, et al. (2008) SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr Biol 18: 1432–1437. doi: 10.1016/j.cub.2008.08.041 18812090
78. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, et al. (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. doi: 10.1111/j.1365-313X.2008.03470.x 18318687
79. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, et al. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8: e1002799. doi: 10.1371/journal.pgen.1002799 22844245
80. Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosom Res 4: 507–516.
81. Armstrong SJ, Caryl APP, Jones GH, Franklin FCH (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645–3655. doi: 10.1242/jcs.00048 12186950
82. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: 2488–2500. doi: 10.1101/gad.354705 16230536
83. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34–41. doi: 10.1263/jbb.104.34 17697981
84. Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, et al. (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20: 2146–2159. doi: 10.1105/tpc.107.056812 18757558
85. Perkins DD (1949) Biochemical mutants in the smut fungus Ustilago Maydis. Genetics 34: 607–626. 17247336
86. Malkova A, Swanson J, German M, McCusker JH, Housworth E a, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49–63. doi: 10.1534/genetics.104.027961 15454526
87. Shinohara M, Sakai K, Shinohara A, Bishop DK (2003) Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics 163: 1273–1286. 12702674
88. Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458–1460. 8197459
89. Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breed 30: 1231–1235. doi: 10.1007/s11032-012-9706-y
90. Kosambi D (1943) The estimation of map distances from recombination values. Ann Eugen 12: 172–175.
91. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279–284. 11682119
92. Zhang D, Rogers GC, Buster DW, Sharp DJ (2007) Three microtubule severing enzymes contribute to the “Pacman-flux” machinery that moves chromosomes. J Cell Biol 177: 231–242. doi: 10.1083/jcb.200612011 17452528
93. Mukherjee S, Diaz Valencia JD, Stewman S, Metz J, Monnier S, et al. (2012) Human fidgetin is a microtubule severing enzyme and minus-end depolymerase that regulates mitosis. Cell Cycle 11: 2359–2366. doi: 10.4161/cc.20849 22672901
94. Cox G a, Mahaffey CL, Nystuen A, Letts V a, Frankel WN (2000) The mouse fidgetin gene defines a new role for AAA family proteins in mammalian development. Nat Genet 26: 198–202. doi: 10.1038/79923 11017077
95. Yang Y, Mahaffey CL, Bérubé N, Nystuen A, Frankel WN (2005) Functional characterization of fidgetin, an AAA-family protein mutated in fidget mice. Exp Cell Res 304: 50–58. doi: 10.1016/j.yexcr.2004.11.014 15707573
96. Yakushiji Y, Yamanaka K, Ogura T (2004) Identification of a cysteine residue important for the ATPase activity of C. elegans fidgetin homologue. FEBS Lett 578: 191–197. 15581640
97. Casanova M, Crobu L, Blaineau C, Bourgeois N, Bastien P, et al. (2009) Microtubule-severing proteins are involved in flagellar length control and mitosis in Trypanosomatids. Mol Microbiol 71: 1353–1370. doi: 10.1111/j.1365-2958.2009.06594.x 19183280
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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