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The chromosome axis controls meiotic events through a hierarchical assembly of HORMA domain proteins.

Kim Y, Rosenberg SC, Kugel CL, Kostow N, Rog O, Davydov V, Su TY, Dernburg AF, Corbett KD
Dev Cell 31 487-502 (2014)
Related entries: 4trk, 4tzl, 4tzm, 4tzn, 4tzo, 4tzq, 4tzs

Cited: 68 times
EuropePMC logo PMID: 25446517

Abstract

Proteins of the HORMA domain family play central, but poorly understood, roles in chromosome organization and dynamics during meiosis. In Caenorhabditis elegans, four such proteins (HIM-3, HTP-1, HTP-2, and HTP-3) have distinct but overlapping functions. Through combined biochemical, structural, and in vivo analysis, we find that these proteins form hierarchical complexes through binding of their HORMA domains to cognate peptides within their partners' C-terminal tails, analogous to the "safety belt" binding mechanism of Mad2. These interactions are critical for recruitment of HIM-3, HTP-1, and HTP-2 to chromosome axes. HTP-3, in addition to recruiting the other HORMA domain proteins to the axis, plays an independent role in sister chromatid cohesion and double-strand break formation. Finally, we find that mammalian HORMAD1 binds a motif found both at its own C terminus and at that of HORMAD2, indicating that this mode of intermolecular association is a conserved feature of meiotic chromosome structure in eukaryotes.

Reviews - 4tzj mentioned but not cited (1)

  1. Disassembly of the Shieldin Complex by TRIP13. Sarangi P, Clairmont CS, D'Andrea AD. Cell Cycle 19 1565-1575 (2020)

Articles - 4tzj mentioned but not cited (2)

  1. TRIP13 is a protein-remodeling AAA+ ATPase that catalyzes MAD2 conformation switching. Ye Q, Rosenberg SC, Moeller A, Speir JA, Su TY, Corbett KD. Elife 4 (2015)
  2. The chromosome axis controls meiotic events through a hierarchical assembly of HORMA domain proteins. Kim Y, Rosenberg SC, Kugel CL, Kostow N, Rog O, Davydov V, Su TY, Dernburg AF, Corbett KD. Dev Cell 31 487-502 (2014)


Reviews citing this publication (18)

  1. The Molecular Biology of Spindle Assembly Checkpoint Signaling Dynamics. Musacchio A. Curr Biol 25 R1002-18 (2015)
  2. The multifaceted roles of the HORMA domain in cellular signaling. Rosenberg SC, Corbett KD. J Cell Biol 211 745-755 (2015)
  3. Zipping and Unzipping: Protein Modifications Regulating Synaptonemal Complex Dynamics. Gao J, Colaiácovo MP. Trends Genet 34 232-245 (2018)
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  6. Meiotic recombination and the crossover assurance checkpoint in Caenorhabditis elegans. Yu Z, Kim Y, Dernburg AF. Semin Cell Dev Biol 54 106-116 (2016)
  7. Insights into a Crucial Role of TRIP13 in Human Cancer. Lu S, Qian J, Guo M, Gu C, Yang Y. Comput Struct Biotechnol J 17 854-861 (2019)
  8. Mechanism and Control of Meiotic DNA Double-Strand Break Formation in S. cerevisiae. Yadav VK, Claeys Bouuaert C. Front Cell Dev Biol 9 642737 (2021)
  9. Chromosome Organization in Early Meiotic Prophase. Grey C, de Massy B. Front Cell Dev Biol 9 688878 (2021)
  10. Let's get physical - mechanisms of crossover interference. von Diezmann L, Rog O. J Cell Sci 134 jcs255745 (2021)
  11. REV7 directs DNA repair pathway choice. Clairmont CS, D'Andrea AD. Trends Cell Biol 31 965-978 (2021)
  12. Intricate Regulatory Mechanisms of the Anaphase-Promoting Complex/Cyclosome and Its Role in Chromatin Regulation. Bodrug T, Welsh KA, Hinkle M, Emanuele MJ, Brown NG. Front Cell Dev Biol 9 687515 (2021)
  13. The organization, regulation, and biological functions of the synaptonemal complex. Zhang FG, Zhang RR, Gao JM. Asian J Androl 23 580-589 (2021)
  14. Phospho-Regulation of Meiotic Prophase. Kar FM, Hochwagen A. Front Cell Dev Biol 9 667073 (2021)
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  16. Building the synaptonemal complex: Molecular interactions between the axis and the central region. Gordon SG, Rog O. PLoS Genet 19 e1010822 (2023)
  17. Divergence and conservation of the meiotic recombination machinery. Arter M, Keeney S. Nat Rev Genet (2023)
  18. REV7 in Cancer Biology and Management. Murakumo Y, Sakurai Y, Kato T, Hashimoto H, Ichinoe M. Cancers (Basel) 15 1721 (2023)

Articles citing this publication (47)

  1. The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors. Rog O, Köhler S, Dernburg AF. Elife 6 e21455 (2017)
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  3. The Chromosome Axis Mediates Feedback Control of CHK-2 to Ensure Crossover Formation in C. elegans. Kim Y, Kostow N, Dernburg AF. Dev Cell 35 247-261 (2015)
  4. Structure of the Human Atg13-Atg101 HORMA Heterodimer: an Interaction Hub within the ULK1 Complex. Qi S, Kim DJ, Stjepanovic G, Hurley JH. Structure 23 1848-1857 (2015)
  5. Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue. Köhler S, Wojcik M, Xu K, Dernburg AF. Proc Natl Acad Sci U S A 114 E4734-E4743 (2017)
  6. Conformational dynamics of the Hop1 HORMA domain reveal a common mechanism with the spindle checkpoint protein Mad2. West AMV, Komives EA, Corbett KD. Nucleic Acids Res 46 279-292 (2018)
  7. Molecular organization of mammalian meiotic chromosome axis revealed by expansion STORM microscopy. Xu H, Tong Z, Ye Q, Sun T, Hong Z, Zhang L, Bortnick A, Cho S, Beuzer P, Axelrod J, Hu Q, Wang M, Evans SM, Murre C, Lu LF, Sun S, Corbett KD, Cang H. Proc Natl Acad Sci U S A 116 18423-18428 (2019)
  8. The AAA+ ATPase TRIP13 remodels HORMA domains through N-terminal engagement and unfolding. Ye Q, Kim DH, Dereli I, Rosenberg SC, Hagemann G, Herzog F, Tóth A, Cleveland DW, Corbett KD. EMBO J 36 2419-2434 (2017)
  9. ASY1 acts as a dosage-dependent antagonist of telomere-led recombination and mediates crossover interference in Arabidopsis. Lambing C, Kuo PC, Tock AJ, Topp SD, Henderson IR. Proc Natl Acad Sci U S A 117 13647-13658 (2020)
  10. Spatiotemporal regulation of Aurora B recruitment ensures release of cohesion during C. elegans oocyte meiosis. Ferrandiz N, Barroso C, Telecan O, Shao N, Kim HM, Testori S, Faull P, Cutillas P, Snijders AP, Colaiácovo MP, Martinez-Perez E. Nat Commun 9 834 (2018)
  11. The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans. Li Q, Saito TT, Martinez-Garcia M, Deshong AJ, Nadarajan S, Lawrence KS, Checchi PM, Colaiacovo MP, Engebrecht J. PLoS Genet 14 e1007701 (2018)
  12. TRIP13PCH-2 promotes Mad2 localization to unattached kinetochores in the spindle checkpoint response. Nelson CR, Hwang T, Chen PH, Bhalla N. J Cell Biol 211 503-516 (2015)
  13. The Arabidopsis Cdk1/Cdk2 homolog CDKA;1 controls chromosome axis assembly during plant meiosis. Yang C, Sofroni K, Wijnker E, Hamamura Y, Carstens L, Harashima H, Stolze SC, Vezon D, Chelysheva L, Orban-Nemeth Z, Pochon G, Nakagami H, Schlögelhofer P, Grelon M, Schnittger A. EMBO J 39 e101625 (2020)
  14. Impeding DNA Break Repair Enables Oocyte Quality Control. Qiao H, Rao HBDP, Yun Y, Sandhu S, Fong JH, Sapre M, Nguyen M, Tham A, Van BW, Chng TYH, Lee A, Hunter N. Mol Cell 72 211-221.e3 (2018)
  15. The Cancer/Testes (CT) Antigen HORMAD1 promotes Homologous Recombinational DNA Repair and Radioresistance in Lung adenocarcinoma cells. Gao Y, Kardos J, Yang Y, Tamir TY, Mutter-Rottmayer E, Weissman B, Major MB, Kim WY, Vaziri C. Sci Rep 8 15304 (2018)
  16. Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation. Sato-Carlton A, Nakamura-Tabuchi C, Chartrand SK, Uchino T, Carlton PM. J Cell Biol 217 555-570 (2018)
  17. The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis. Nadarajan S, Mohideen F, Tzur YB, Ferrandiz N, Crawley O, Montoya A, Faull P, Snijders AP, Cutillas PR, Jambhekar A, Blower MD, Martinez-Perez E, Harper JW, Colaiacovo MP. Elife 5 e12039 (2016)
  18. Identification of novel synaptonemal complex components in C. elegans. Hurlock ME, Čavka I, Kursel LE, Haversat J, Wooten M, Nizami Z, Turniansky R, Hoess P, Ries J, Gall JG, Rog O, Köhler S, Kim Y. J Cell Biol 219 e201910043 (2020)
  19. Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis. Medhi D, Goldman AS, Lichten M. Elife 5 e19669 (2016)
  20. Chromosome-autonomous feedback down-regulates meiotic DNA break competence upon synaptonemal complex formation. Mu X, Murakami H, Mohibullah N, Keeney S. Genes Dev 34 1605-1618 (2020)
  21. Quantitative cytogenetics reveals molecular stoichiometry and longitudinal organization of meiotic chromosome axes and loops. Woglar A, Yamaya K, Roelens B, Boettiger A, Köhler S, Villeneuve AM. PLoS Biol 18 e3000817 (2020)
  22. Conserved HORMA domain-containing protein Hop1 stabilizes interaction between proteins of meiotic DNA break hotspots and chromosome axis. Kariyazono R, Oda A, Yamada T, Ohta K. Nucleic Acids Res 47 10166-10180 (2019)
  23. Histone H3K4 methylation regulates deactivation of the spindle assembly checkpoint through direct binding of Mad2. Schibler A, Koutelou E, Tomida J, Wilson-Pham M, Wang L, Lu Y, Cabrera AP, Chosed RJ, Li W, Li B, Shi X, Wood RD, Dent SY. Genes Dev 30 1187-1197 (2016)
  24. Observation of Extensive Chromosome Axis Remodeling during the "Diffuse-Phase" of Meiosis in Large Genome Cereals. Colas I, Darrier B, Arrieta M, Mittmann SU, Ramsay L, Sourdille P, Waugh R. Front Plant Sci 8 1235 (2017)
  25. State changes of the HORMA protein ASY1 are mediated by an interplay between its closure motif and PCH2. Yang C, Hu B, Portheine SM, Chuenban P, Schnittger A. Nucleic Acids Res 48 11521-11535 (2020)
  26. The conserved LEM-3/Ankle1 nuclease is involved in the combinatorial regulation of meiotic recombination repair and chromosome segregation in Caenorhabditis elegans. Hong Y, Velkova M, Silva N, Jagut M, Scheidt V, Labib K, Jantsch V, Gartner A. PLoS Genet 14 e1007453 (2018)
  27. Synaptonemal Complex Components Are Required for Meiotic Checkpoint Function in Caenorhabditis elegans. Bohr T, Ashley G, Eggleston E, Firestone K, Bhalla N. Genetics 204 987-997 (2016)
  28. A first genetic portrait of synaptonemal complex variation. Wang RJ, Dumont BL, Jing P, Payseur BA. PLoS Genet 15 e1008337 (2019)
  29. Caenorhabditis elegans DSB-3 reveals conservation and divergence among protein complexes promoting meiotic double-strand breaks. Hinman AW, Yeh HY, Roelens B, Yamaya K, Woglar A, Bourbon HG, Chi P, Villeneuve AM. Proc Natl Acad Sci U S A 118 e2109306118 (2021)
  30. Surveillance of cohesin-supported chromosome structure controls meiotic progression. Castellano-Pozo M, Pacheco S, Sioutas G, Jaso-Tamame AL, Dore MH, Karimi MM, Martinez-Perez E. Nat Commun 11 4345 (2020)
  31. PCH-2 collaborates with CMT-1 to proofread meiotic homolog interactions. Giacopazzi S, Vong D, Devigne A, Bhalla N. PLoS Genet 16 e1008904 (2020)
  32. Pch2 orchestrates the meiotic recombination checkpoint from the cytoplasm. Herruzo E, Lago-Maciel A, Baztán S, Santos B, Carballo JA, San-Segundo PA. PLoS Genet 17 e1009560 (2021)
  33. Novel mechanistic insights into the role of Mer2 as the keystone of meiotic DNA break formation. Rousová D, Nivsarkar V, Altmannova V, Raina VB, Funk SK, Liedtke D, Janning P, Müller F, Reichle H, Vader G, Weir JR. Elife 10 e72330 (2021)
  34. Phosphoregulation of HORMA domain protein HIM-3 promotes asymmetric synaptonemal complex disassembly in meiotic prophase in Caenorhabditis elegans. Sato-Carlton A, Nakamura-Tabuchi C, Li X, Boog H, Lehmer MK, Rosenberg SC, Barroso C, Martinez-Perez E, Corbett KD, Carlton PM. PLoS Genet 16 e1008968 (2020)
  35. Genetic interactions between the chromosome axis-associated protein Hop1 and homologous recombination determinants in Schizosaccharomyces pombe. Brown SD, Jarosinska OD, Lorenz A. Curr Genet 64 1089-1104 (2018)
  36. Closing the Mad2 cycle. Musacchio A. Elife 4 (2015)
  37. Shugoshin Is Essential for Meiotic Prophase Checkpoints in C. elegans. Bohr T, Nelson CR, Giacopazzi S, Lamelza P, Bhalla N. Curr Biol 28 3199-3211.e3 (2018)
  38. A small RNA system ensures accurate homologous pairing and unpaired silencing of meiotic chromosomes. Tabara H, Mitani S, Mochizuki M, Kohara Y, Nagata K. EMBO J 42 e105002 (2023)
  39. Single-Molecule Tracking of Chromatin-Associated Proteins in the C. elegans Gonad. von Diezmann L, Rog O. J Phys Chem B 125 6162-6170 (2021)
  40. Turning coldspots into hotspots: targeted recruitment of axis protein Hop1 stimulates meiotic recombination in Saccharomyces cerevisiae. Shodhan A, Xaver M, Wheeler D, Lichten M. Genetics 222 iyac106 (2022)
  41. A suppressor screen in C. elegans identifies a multiprotein interaction that stabilizes the synaptonemal complex. Kursel LE, Martinez JEA, Rog O. Proc Natl Acad Sci U S A 120 e2314335120 (2023)
  42. Comparative genomics of HORMA domain-containing proteins in prokaryotes and eukaryotes. Almutairi ZM. Cell Cycle 17 2531-2546 (2018)
  43. Does the Pachytene Checkpoint, a Feature of Meiosis, Filter Out Mistakes in Double-Strand DNA Break Repair and as a side-Effect Strongly Promote Adaptive Speciation? Foe VE. Integr Org Biol 4 obac008 (2022)
  44. Meiosis in budding yeast. Börner GV, Hochwagen A, MacQueen AJ. Genetics 225 iyad125 (2023)
  45. TOP-2 is differentially required for the proper maintenance of the cohesin subunit REC-8 on meiotic chromosomes in Caenorhabditis elegans spermatogenesis and oogenesis. Rourke C, Jaramillo-Lambert A. Genetics 222 iyac120 (2022)
  46. The conserved AAA ATPase PCH-2 distributes its regulation of meiotic prophase events through multiple meiotic HORMADs in C. elegans. Russo AE, Giacopazzi S, Deshong A, Menon M, Ortiz V, Ego KM, Corbett KD, Bhalla N. PLoS Genet 19 e1010708 (2023)
  47. The dynamic recruitment of LAB proteins senses meiotic chromosome axis differentiation in C. elegans. Wang R, Li J, Tian Y, Sun Y, Zhang Y, Liu M, Zhang R, Zhao L, Li Q, Meng X, Zhou J, Gao J. J Cell Biol 223 e202212035 (2024)


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