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Dynamic feature of mitotic arrest deficient 2-like protein 2 (MAD2L2) and structural basis for its interaction with chromosome alignment-maintaining phosphoprotein (CAMP).

Hara K, Taharazako S, Ikeda M, Fujita H, Mikami Y, Kikuchi S, Hishiki A, Yokoyama H, Ishikawa Y, Kanno SI, Tanaka K, Hashimoto H
J Biol Chem 292 17658-17667 (2017)
Cited: 26 times
EuropePMC logo PMID: 28887307

Abstract

Mitotic arrest deficient 2-like protein 2 (MAD2L2), also termed MAD2B or REV7, is involved in multiple cellular functions including translesion DNA synthesis (TLS), signal transduction, transcription, and mitotic events. MAD2L2 interacts with chromosome alignment-maintaining phosphoprotein (CAMP), a kinetochore-microtubule attachment protein in mitotic cells, presumably through a novel "WK" motif in CAMP. Structures of MAD2L2 in complex with binding regions of the TLS proteins REV3 and REV1 have revealed that MAD2L2 has two faces for protein-protein interactions that are regulated by its C-terminal region; however, the mechanisms underlying the MAD2L2-CAMP interaction and the mitotic role of MAD2L2 remain unknown. Here we have determined the structures of human MAD2L2 in complex with a CAMP fragment in two crystal forms. The overall structure of the MAD2L2-CAMP complex in both crystal forms was essentially similar to that of the MAD2L2-REV3 complex. However, the residue interactions between MAD2L2 and CAMP were strikingly different from those in the MAD2L2-REV3 complex. Furthermore, structure-based interaction analyses revealed an unprecedented mechanism involving CAMP's WK motif. Surprisingly, in one of the crystal forms, the MAD2L2-CAMP complex formed a dimeric structure in which the C-terminal region of MAD2L2 was swapped and adopted an immature structure. The structure provides direct evidence for the dynamic nature of MAD2L2 structure, which in turn may have implications for the protein-protein interaction mechanism and the multiple functions of this protein. This work is the first structural study of MAD2L2 aside from its role in TLS and might pave the way to clarify MAD2L2's function in mitosis.

Reviews - 5xpu mentioned but not cited (1)

  1. Fanconi anemia pathway as a prospective target for cancer intervention. Liu W, Palovcak A, Li F, Zafar A, Yuan F, Zhang Y. Cell Biosci 10 39 (2020)

Articles - 5xpu mentioned but not cited (1)

  1. Dynamic feature of mitotic arrest deficient 2-like protein 2 (MAD2L2) and structural basis for its interaction with chromosome alignment-maintaining phosphoprotein (CAMP). Hara K, Taharazako S, Ikeda M, Fujita H, Mikami Y, Kikuchi S, Hishiki A, Yokoyama H, Ishikawa Y, Kanno SI, Tanaka K, Hashimoto H. J Biol Chem 292 17658-17667 (2017)


Reviews citing this publication (9)

  1. DNA polymerase ζ in DNA replication and repair. Martin SK, Wood RD. Nucleic Acids Res 47 8348-8361 (2019)
  2. REV7 directs DNA repair pathway choice. Clairmont CS, D'Andrea AD. Trends Cell Biol 31 965-978 (2021)
  3. REV7: Jack of many trades. de Krijger I, Boersma V, Jacobs JJL. Trends Cell Biol 31 686-701 (2021)
  4. Targeting protein-protein interactions in the DNA damage response pathways for cancer chemotherapy. McPherson KS, Korzhnev DM. RSC Chem Biol 2 1167-1195 (2021)
  5. Disassembly of the Shieldin Complex by TRIP13. Sarangi P, Clairmont CS, D'Andrea AD. Cell Cycle 19 1565-1575 (2020)
  6. Functions and Regulation of Meiotic HORMA-Domain Proteins. Prince JP, Martinez-Perez E. Genes (Basel) 13 777 (2022)
  7. Structural basis for the molecular interactions in DNA damage tolerances. Hashimoto H, Hishiki A, Hara K, Kikuchi S. Biophys Physicobiol 14 199-205 (2017)
  8. REV7 in Cancer Biology and Management. Murakumo Y, Sakurai Y, Kato T, Hashimoto H, Ichinoe M. Cancers (Basel) 15 1721 (2023)
  9. [Structural Basis of the Multifunctional Hub Protein and Identification of a Small-molecule Compound for Drug Discovery]. Hara K. Yakugaku Zasshi 139 969-973 (2019)

Articles citing this publication (15)

  1. TRIP13 regulates DNA repair pathway choice through REV7 conformational change. Clairmont CS, Sarangi P, Ponnienselvan K, Galli LD, Csete I, Moreau L, Adelmant G, Chowdhury D, Marto JA, D'Andrea AD. Nat Cell Biol 22 87-96 (2020)
  2. FAM35A associates with REV7 and modulates DNA damage responses of normal and BRCA1-defective cells. Tomida J, Takata KI, Bhetawal S, Person MD, Chao HP, Tang DG, Wood RD. EMBO J 37 e99543 (2018)
  3. Molecular basis for assembly of the shieldin complex and its implications for NHEJ. Liang L, Feng J, Zuo P, Yang J, Lu Y, Yin Y. Nat Commun 11 1972 (2020)
  4. Structural basis for shieldin complex subunit 3-mediated recruitment of the checkpoint protein REV7 during DNA double-strand break repair. Dai Y, Zhang F, Wang L, Shan S, Gong Z, Zhou Z. J Biol Chem 295 250-262 (2020)
  5. Molecular mechanisms of assembly and TRIP13-mediated remodeling of the human Shieldin complex. Xie W, Wang S, Wang J, de la Cruz MJ, Xu G, Scaltriti M, Patel DJ. Proc Natl Acad Sci U S A 118 e2024512118 (2021)
  6. REV7 has a dynamic adaptor region to accommodate small GTPase RAN/Shigella IpaB ligands, and its activity is regulated by the RanGTP/GDP switch. Wang X, Pernicone N, Pertz L, Hua D, Zhang T, Listovsky T, Xie W. J Biol Chem 294 15733-15742 (2019)
  7. MAD2L2 dimerization and TRIP13 control shieldin activity in DNA repair. de Krijger I, Föhr B, Pérez SH, Vincendeau E, Serrat J, Thouin AM, Susvirkar V, Lescale C, Paniagua I, Hoekman L, Kaur S, Altelaar M, Deriano L, Faesen AC, Jacobs JJL. Nat Commun 12 5421 (2021)
  8. CHAMP1-POGZ counteracts the inhibitory effect of 53BP1 on homologous recombination and affects PARP inhibitor resistance. Fujita H, Ikeda M, Ui A, Ouchi Y, Mikami Y, Kanno SI, Yasui A, Tanaka K. Oncogene 41 2706-2718 (2022)
  9. CHAMP1 binds to REV7/FANCV and promotes homologous recombination repair. Li F, Sarangi P, Iyer DR, Feng H, Moreau L, Nguyen H, Clairmont C, D'Andrea AD. Cell Rep 40 111297 (2022)
  10. Chromosome alignment-maintaining phosphoprotein CHAMP1 plays a role in cell survival through regulating Mcl-1 expression. Hino M, Iemura K, Ikeda M, Itoh G, Tanaka K. Cancer Sci 112 3711-3721 (2021)
  11. Transcriptional and Histochemical Signatures of Bone Marrow Mononuclear Cell-Mediated Resolution of Synovitis. Menarim BC, El-Sheikh Ali H, Loux SC, Scoggin KE, Kalbfleisch TS, MacLeod JN, Dahlgren LA. Front Immunol 12 734322 (2021)
  12. Disrupting the MAD2L2-Rev1 Complex Enhances Cell Death upon DNA Damage. Pernicone N, Elias M, Onn I, Tobi D, Listovsky T. Molecules 27 636 (2022)
  13. Oxaliplatin promotes siMAD2L2‑induced apoptosis in colon cancer cells. Ma L, Li X, Zhao X, Sun H, Kong F, Li Y, Sui Y, Xu F. Mol Med Rep 24 629 (2021)
  14. Evolution of Rev7 interactions in eukaryotic TLS DNA polymerase Polζ. McPherson KS, Rizzo AA, Erlandsen H, Chatterjee N, Walker GC, Korzhnev DM. J Biol Chem 299 102859 (2023)
  15. Identification of a Novel CD8+ T cell exhaustion-related gene signature for predicting survival in hepatocellular carcinoma. Liu K, Liu J, Zhang X, Liu D, Yao W, Bu Y, Chen B. BMC Cancer 23 1185 (2023)


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