PCH-2 collaborates with CMT-1 to proofread meiotic homolog interactions


Autoři: Stefani Giacopazzi aff001;  Daniel Vong aff001;  Alice Devigne aff001;  Needhi Bhalla aff001
Působiště autorů: Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America aff001
Vyšlo v časopise: PCH-2 collaborates with CMT-1 to proofread meiotic homolog interactions. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008904
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008904

Souhrn

The conserved ATPase, PCH-2/TRIP13, is required during both the spindle checkpoint and meiotic prophase. However, its specific role in regulating meiotic homolog pairing, synapsis and recombination has been enigmatic. Here, we report that this enzyme is required to proofread meiotic homolog interactions. We generated a mutant version of PCH-2 in C. elegans that binds ATP but cannot hydrolyze it: pch-2E253Q. In vitro, this mutant can bind a known substrate but is unable to remodel it. This mutation results in some non-homologous synapsis and impaired crossover assurance. Surprisingly, worms with a null mutation in PCH-2’s adapter protein, CMT-1, the ortholog of p31comet, localize PCH-2 to meiotic chromosomes, exhibit non-homologous synapsis and lose crossover assurance. The similarity in phenotypes between cmt-1 and pch-2E253Q mutants suggest that PCH-2 can bind its meiotic substrates in the absence of CMT-1, in contrast to its role during the spindle checkpoint, but requires its adapter to hydrolyze ATP and remodel them.

Klíčová slova:

Apoptosis – Caenorhabditis elegans – DNA repair – Homologous chromosomes – Homologous recombination – Meiotic prophase – Nuclear staining – Synapsis


Zdroje

1. Bhalla N, Dernburg AF. Prelude to a division. Annu Rev Cell Dev Biol. 2008;24:397–424. doi: 10.1146/annurev.cellbio.23.090506.123245 18597662; PubMed Central PMCID: PMC4435778.

2. Borner GV, Kleckner N, Hunter N. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell. 2004;117(1):29–45. doi: 10.1016/s0092-8674(04)00292-2 15066280.

3. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, et al. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell. 2003;5(3):463–74. doi: 10.1016/s1534-5807(03)00232-6 12967565.

4. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, et al. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 2005;19(11):1376–89. doi: 10.1101/gad.329705 15937223; PubMed Central PMCID: PMC1142560.

5. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 2005;19(20):2488–500. doi: 10.1101/gad.354705 16230536; PubMed Central PMCID: PMC1257403.

6. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–42. doi: 10.1101/gad.1011602 12231631.

7. Page SL, Hawley RS. c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 2001;15(23):3130–43. doi: 10.1101/gad.935001 11731477; PubMed Central PMCID: PMC312841.

8. Sym M, Engebrecht JA, Roeder GS. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993;72(3):365–78. doi: 10.1016/0092-8674(93)90114-6 7916652.

9. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000;6(5):989–98. doi: 10.1016/s1097-2765(00)00098-8 11106739.

10. Gerton JL, DeRisi JL. Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc Natl Acad Sci U S A. 2002;99(10):6895–900. doi: 10.1073/pnas.102167899 12011448; PubMed Central PMCID: PMC124500.

11. Ku JC, Ronceret A, Golubovskaya I, Lee DH, Wang C, Timofejeva L, et al. Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis. PLoS Genet. 2020;16(4):e1007881. doi: 10.1371/journal.pgen.1007881 32310948.

12. Leu JY, Chua PR, Roeder GS. The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell. 1998;94(3):375–86. doi: 10.1016/s0092-8674(00)81480-4 9708739.

13. Petukhova GV, Romanienko PJ, Camerini-Otero RD. The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev Cell. 2003;5(6):927–36. doi: 10.1016/s1534-5807(03)00369-1 14667414.

14. Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell. 2000;6(5):975–87. doi: 10.1016/s1097-2765(00)00097-6 11106738.

15. Tsubouchi H, Roeder GS. The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol Cell Biol. 2002;22(9):3078–88. doi: 10.1128/mcb.22.9.3078-3088.2002 11940665; PubMed Central PMCID: PMC133769.

16. Tsubouchi H, Roeder GS. The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell. 2003;5(6):915–25. doi: 10.1016/s1534-5807(03)00357-5 14667413.

17. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell. 1998;1(5):707–18. doi: 10.1016/s1097-2765(00)80070-2 9660954.

18. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell. 1998;94(3):387–98. doi: 10.1016/s0092-8674(00)81481-6 9708740.

19. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, et al. Meiotic synapsis in the absence of recombination. Science. 1998;279(5352):876–8. doi: 10.1126/science.279.5352.876 9452390.

20. Couteau F, Nabeshima K, Villeneuve A, Zetka M. A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol. 2004;14(7):585–92. doi: 10.1016/j.cub.2004.03.033 15062099.

21. Couteau F, Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005;19(22):2744–56. doi: 10.1101/gad.1348205 16291647; PubMed Central PMCID: PMC1283966.

22. Martinez-Perez E, Villeneuve AM. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19(22):2727–43. doi: 10.1101/gad.1338505 16291646; PubMed Central PMCID: PMC1283965.

23. Silva N, Ferrandiz N, Barroso C, Tognetti S, Lightfoot J, Telecan O, et al. The fidelity of synaptonemal complex assembly is regulated by a signaling mechanism that controls early meiotic progression. Dev Cell. 2014;31(4):503–11. doi: 10.1016/j.devcel.2014.10.001 25455309.

24. Labrador L, Barroso C, Lightfoot J, Muller-Reichert T, Flibotte S, Taylor J, et al. Chromosome movements promoted by the mitochondrial protein SPD-3 are required for homology search during Caenorhabditis elegans meiosis. PLoS Genet. 2013;9(5):e1003497. doi: 10.1371/journal.pgen.1003497 23671424; PubMed Central PMCID: PMC3649994.

25. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, Gruenbaum Y, et al. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell. 2007;12(6):873–85. doi: 10.1016/j.devcel.2007.05.004 17543861.

26. Hatkevich T, Boudreau V, Rubin T, Maddox PS, Huynh JR, Sekelsky J. Centromeric SMC1 promotes centromere clustering and stabilizes meiotic homolog pairing. PLoS Genet. 2019;15(10):e1008412. doi: 10.1371/journal.pgen.1008412 31609962; PubMed Central PMCID: PMC6812850.

27. Dombecki CR, Chiang AC, Kang HJ, Bilgir C, Stefanski NA, Neva BJ, et al. The chromodomain protein MRG-1 facilitates SC-independent homologous pairing during meiosis in Caenorhabditis elegans. Dev Cell. 2011;21(6):1092–103. doi: 10.1016/j.devcel.2011.09.019 22172672.

28. Borner GV, Barot A, Kleckner N. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A. 2008;105(9):3327–32. doi: 10.1073/pnas.0711864105 18305165; PubMed Central PMCID: PMC2265181.

29. Chen C, Jomaa A, Ortega J, Alani EE. Pch2 is a hexameric ring ATPase that remodels the chromosome axis protein Hop1. Proc Natl Acad Sci U S A. 2014;111(1):E44–53. doi: 10.1073/pnas.1310755111 24367111; PubMed Central PMCID: PMC3890899.

30. Joshi N, Barot A, Jamison C, Borner GV. Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet. 2009;5(7):e1000557. doi: 10.1371/journal.pgen.1000557 19629172; PubMed Central PMCID: PMC2708914.

31. Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD, Copenhaver GP, et al. Arabidopsis PCH2 Mediates Meiotic Chromosome Remodeling and Maturation of Crossovers. PLoS Genet. 2015;11(7):e1005372. doi: 10.1371/journal.pgen.1005372 26182244; PubMed Central PMCID: PMC4504720.

32. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, 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(10):e1000702. doi: 10.1371/journal.pgen.1000702 19851446; PubMed Central PMCID: PMC2758600.

33. Bohr T, Ashley G, Eggleston E, Firestone K, Bhalla N. Synaptonemal Complex Components Are Required for Meiotic Checkpoint Function in Caenorhabditis elegans. Genetics. 2016;204(3):987–97. doi: 10.1534/genetics.116.191494 27605049; PubMed Central PMCID: PMC5105873.

34. Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, et al. Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol. 2011;13(5):599–610. doi: 10.1038/ncb2213 21478856; PubMed Central PMCID: PMC3087846.

35. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell. 2008;14(2):263–74. doi: 10.1016/j.devcel.2007.11.016 18267094.

36. Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2 2107981.

37. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 2007;21(17):2220–33. doi: 10.1101/gad.439007 17785529; PubMed Central PMCID: PMC1950860.

38. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, et al. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet. 2010;6(11):e1001190. doi: 10.1371/journal.pgen.1001190 21079677; PubMed Central PMCID: PMC2973818.

39. Shin YH, McGuire MM, Rajkovic A. Mouse HORMAD1 is a meiosis i checkpoint protein that modulates DNA double- strand break repair during female meiosis. Biol Reprod. 2013;89(2):29. doi: 10.1095/biolreprod.112.106773 23759310; PubMed Central PMCID: PMC4076362.

40. Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, Fu J, et al. Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev. 2012;26(9):958–73. doi: 10.1101/gad.187559.112 22549958; PubMed Central PMCID: PMC3347793.

41. Zetka MC, Kawasaki I, Strome S, Muller 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(17):2258–70. doi: 10.1101/gad.13.17.2258 10485848; PubMed Central PMCID: PMC317003.

42. Aravind L, Koonin EV. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci. 1998;23(8):284–6. doi: 10.1016/s0968-0004(98)01257-2 9757827.

43. Rosenberg SC, Corbett KD. The multifaceted roles of the HORMA domain in cellular signaling. J Cell Biol. 2015;211(4):745–55. doi: 10.1083/jcb.201509076 26598612; PubMed Central PMCID: PMC4657174.

44. Vader G. Pch2(TRIP13): controlling cell division through regulation of HORMA domains. Chromosoma. 2015;124(3):333–9. doi: 10.1007/s00412-015-0516-y 25895724.

45. Kim Y, Rosenberg SC, Kugel CL, Kostow N, Rog O, Davydov V, et al. The chromosome axis controls meiotic events through a hierarchical assembly of HORMA domain proteins. Dev Cell. 2014;31(4):487–502. doi: 10.1016/j.devcel.2014.09.013 25446517; PubMed Central PMCID: PMC4254552.

46. West AMV, Komives EA, Corbett KD. Conformational dynamics of the Hop1 HORMA domain reveal a common mechanism with the spindle checkpoint protein Mad2. Nucleic Acids Res. 2017. doi: 10.1093/nar/gkx1196 29186573.

47. Medhi D, Goldman AS, Lichten M. Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis. Elife. 2016;5. doi: 10.7554/eLife.19669 27855779; PubMed Central PMCID: PMC5222560.

48. Shodhan A, Medhi D, Lichten M. Noncanonical Contributions of MutLgamma to VDE-Initiated Crossovers During Saccharomyces cerevisiae Meiosis. G3 (Bethesda). 2019;9(5):1647–54. doi: 10.1534/g3.119.400150 30902890; PubMed Central PMCID: PMC6505156.

49. Zanders S, Sonntag Brown M, Chen C, Alani E. Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae. Genetics. 2011;188(3):511–21. doi: 10.1534/genetics.111.129031 21515575; PubMed Central PMCID: PMC3176543.

50. Deshong AJ, Ye AL, Lamelza P, Bhalla N. A quality control mechanism coordinates meiotic prophase events to promote crossover assurance. PLoS Genet. 2014;10(4):e1004291. doi: 10.1371/journal.pgen.1004291 24762417; PubMed Central PMCID: PMC3998905.

51. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods. 2013;10(10):1028–34. doi: 10.1038/nmeth.2641 23995389; PubMed Central PMCID: PMC3905680.

52. Paix A, Wang Y, Smith HE, Lee CY, Calidas D, Lu T, et al. Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 Sites in Caenorhabditis elegans. Genetics. 2014;198(4):1347–56. doi: 10.1534/genetics.114.170423 25249454; PubMed Central PMCID: PMC4256755.

53. Ye Q, Rosenberg SC, Moeller A, Speir JA, Su TY, Corbett KD. TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching. eLife. 2015;4. Epub 2015/04/29. doi: 10.7554/eLife.07367 25918846; PubMed Central PMCID: PMC4439613.

54. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell. 2005;123(6):1037–50. doi: 10.1016/j.cell.2005.09.034 16360034; PubMed Central PMCID: PMC4435800.

55. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, et al. HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell. 2005;123(6):1051–63. doi: 10.1016/j.cell.2005.09.035 16360035; PubMed Central PMCID: PMC4435792.

56. Phillips CM, Dernburg AF. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell. 2006;11(6):817–29. doi: 10.1016/j.devcel.2006.09.020 17141157.

57. Alpi A, Pasierbek P, Gartner A, Loidl J. Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma. 2003;112(1):6–16. doi: 10.1007/s00412-003-0237-5 12684824.

58. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012;149(1):75–87. doi: 10.1016/j.cell.2012.01.052 22464324; PubMed Central PMCID: PMC3339199.

59. Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, et al. 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(8):e1003674. doi: 10.1371/journal.pgen.1003674 23950729; PubMed Central PMCID: PMC3738457.

60. Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 2013;9(8):e1003679. doi: 10.1371/journal.pgen.1003679 23990794; PubMed Central PMCID: PMC3749324.

61. Alfieri C, Chang L, Barford D. Mechanism for remodelling of the cell cycle checkpoint protein MAD2 by the ATPase TRIP13. Nature. 2018;559(7713):274–8. doi: 10.1038/s41586-018-0281-1 29973720; PubMed Central PMCID: PMC6057611.

62. Brulotte ML, Jeong BC, Li F, Li B, Yu EB, Wu Q, et al. Mechanistic insight into TRIP13-catalyzed Mad2 structural transition and spindle checkpoint silencing. Nat Commun. 2017;8(1):1956. doi: 10.1038/s41467-017-02012-2 29208896; PubMed Central PMCID: PMC5717197.

63. Ji J, Tang D, Shen Y, Xue Z, Wang H, Shi W, et al. P31comet, a member of the synaptonemal complex, participates in meiotic DSB formation in rice. Proc Natl Acad Sci U S A. 2016;113(38):10577–82. doi: 10.1073/pnas.1607334113 27601671; PubMed Central PMCID: PMC5035842.

64. Bhalla N, Dernburg AF. A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science. 2005;310(5754):1683–6. doi: 10.1126/science.1117468 16339446.

65. Bohr T, Nelson CR, Klee E, Bhalla N. Spindle assembly checkpoint proteins regulate and monitor meiotic synapsis in C. elegans. J Cell Biol. 2015;211(2):233–42. doi: 10.1083/jcb.201409035 26483555; PubMed Central PMCID: PMC4621841.

66. Nelson CR, Hwang T, Chen PH, Bhalla N. TRIP13PCH-2 promotes Mad2 localization to unattached kinetochores in the spindle checkpoint response. J Cell Biol. 2015;211(3):503–16. doi: 10.1083/jcb.201505114 26527744; PubMed Central PMCID: PMC4639874.

67. Ma HT, Poon RY. TRIP13 Regulates Both the Activation and Inactivation of the Spindle-Assembly Checkpoint. Cell Rep. 2016;14(5):1086–99. doi: 10.1016/j.celrep.2016.01.001 26832417.

68. Ma HT, Poon RYC. TRIP13 Functions in the Establishment of the Spindle Assembly Checkpoint by Replenishing O-MAD2. Cell Rep. 2018;22(6):1439–50. doi: 10.1016/j.celrep.2018.01.027 29425500.

69. Joyce EF, McKim KS. Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet. 2010;6(8). doi: 10.1371/journal.pgen.1001059 20711363; PubMed Central PMCID: PMC2920846.

70. Rosu S, Libuda DE, Villeneuve AM. Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science. 2011;334(6060):1286–9. doi: 10.1126/science.1212424 22144627; PubMed Central PMCID: PMC3360972.

71. Miniowitz-Shemtov S, Eytan E, Kaisari S, Sitry-Shevah D, Hershko A. Mode of interaction of TRIP13 AAA-ATPase with the Mad2-binding protein p31comet and with mitotic checkpoint complexes. Proc Natl Acad Sci U S A. 2015;112(37):11536–40. doi: 10.1073/pnas.1515358112 26324890; PubMed Central PMCID: PMC4577139.

72. San-Segundo PA, Roeder GS. Pch2 links chromatin silencing to meiotic checkpoint control. Cell. 1999;97(3):313–24. doi: 10.1016/s0092-8674(00)80741-2 10319812.

73. van Hooff JJ, Tromer E, van Wijk LM, Snel B, Kops GJ. Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Rep. 2017. doi: 10.15252/embr.201744102 28642229.

74. Vleugel M, Hoogendoorn E, Snel B, Kops GJ. Evolution and function of the mitotic checkpoint. Dev Cell. 2012;23(2):239–50. doi: 10.1016/j.devcel.2012.06.013 22898774.

75. Tromer EC, van Hooff JJE, Kops G, Snel B. Mosaic origin of the eukaryotic kinetochore. Proc Natl Acad Sci U S A. 2019;116(26):12873–82. doi: 10.1073/pnas.1821945116 31127038; PubMed Central PMCID: PMC6601020.

76. Ye Q, Lau RK, Mathews IT, Birkholz EA, Watrous JD, Azimi CS, et al. HORMA Domain Proteins and a Trip13-like ATPase Regulate Bacterial cGAS-like Enzymes to Mediate Bacteriophage Immunity. Mol Cell. 2020;77(4):709–22 e7. doi: 10.1016/j.molcel.2019.12.009 31932165; PubMed Central PMCID: PMC7036143.

77. Burroughs AM, Zhang D, Schaffer DE, Iyer LM, Aravind L. Comparative genomic analyses reveal a vast, novel network of nucleotide-centric systems in biological conflicts, immunity and signaling. Nucleic Acids Res. 2015;43(22):10633–54. doi: 10.1093/nar/gkv1267 26590262; PubMed Central PMCID: PMC4678834.

78. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94. 4366476; PubMed Central PMCID: PMC1213120.


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 7

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se