Notch-Jagged complex structure implicates a catch bond in tuning ligand sensitivity

Luca, Vincent C.; Kim, Byoung Choul; Ge, Chenghao; Kakuda, Shinako; Wu, Di; Roein-Peikar, Mehdi; Haltiwanger, Robert S.; Zhu, Cheng; Ha, Taekjip; Garcia, K. Christopher

doi:10.1126/science.aaf9739

Title: Notch-Jagged complex structure implicates a catch bond in tuning ligand sensitivity

Journal Article · 01 March 2017 · Science

DOI: https://doi.org/10.1126/science.aaf9739 · OSTI ID:1360203

^[1]; Kim, Byoung Choul ^[2];

^[3]; Kakuda, Shinako ^[4];

^[1]; Roein-Peikar, Mehdi ^[5]; Haltiwanger, Robert S. ^[4];

^[6]; Ha, Taekjip ^[5];

^[1]

Stanford Univ., CA (United States). School of Medicine, Dept. of Molecular and Cellular Physiology and Structural Biology; Howard Hughes Medical Inst., Stanford, CA (United States)
Howard Hughes Medical Inst., Baltimore, MD (United States); Johns Hopkins Univ., Baltimore, MD (United States). Dept. of Biomedical Engineering
Georgia Inst. of Technology, Atlanta, GA (United States). Dept. of Biomedical Engineering
Stony Brook Univ., NY (United States). Dept. of Biochemistry and Cell Biology
Howard Hughes Medical Inst., Baltimore, MD (United States); Johns Hopkins Univ., Baltimore, MD (United States). Dept. of Biomedical Engineering; Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine, Dept. of Biophysics and Biophysical Chemistry
Georgia Inst. of Technology, Atlanta, GA (United States). Woodruff School of Mechanical Engineering, Dept. of Biomedical Engineering

Notch receptor activation initiates cell fate decisions and is distinctive in its reliance on mechanical force and protein glycosylation. The 2.5-angstrom-resolution crystal structure of the extracellular interacting region of Notch1 complexed with an engineered, high-affinity variant of Jagged1 (Jag1) reveals a binding interface that extends ~120 angstroms along five consecutive domains of each protein. O-Linked fucose modifications on Notch1 epidermal growth factor–like (EGF) domains 8 and 12 engage the EGF3 and C2 domains of Jag1, respectively, and different Notch1 domains are favored in binding to Jag1 than those that bind to the Delta-like 4 ligand. Jag1 undergoes conformational changes upon Notch binding, exhibiting catch bond behavior that prolongs interactions in the range of forces required for Notch activation. In conclusion, this mechanism enables cellular forces to regulate binding, discriminate among Notch ligands, and potentiate Notch signaling.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1360203

Journal Information:: Science, Journal Name: Science Journal Issue: 6331 Vol. 355; ISSN 0036-8075

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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Structural and functional dissection of the interplay between lipid and Notch binding by human Notch ligands Suckling, Richard J.; Korona, Boguslawa; Whiteman, Pat The EMBO Journal, Vol. 36, Issue 15 https://doi.org/10.15252/embj.201796632	journal	June 2017
Somatic mutant clones colonize the human esophagus with age. Martincorena, Iñigo; Fowler, Joanna C.; Wabik, Agnieszka Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.31457	text	January 2018
Novel JAG1 Deletion Variant in Patient with Atypical Alagille Syndrome Micaglio, Emanuele; Andronache, Andreea Alina; Carrera, Paola International Journal of Molecular Sciences, Vol. 20, Issue 24 https://doi.org/10.3390/ijms20246247	journal	December 2019
Structural Divergence in O-GlcNAc Glycans Displayed on Epidermal Growth Factor-like Repeats of Mammalian Notch1 Ogawa, Mitsutaka; Senoo, Yuya; Ikeda, Kazutaka Molecules, Vol. 23, Issue 7 https://doi.org/10.3390/molecules23071745	journal	July 2018
Mechanosensitivity of Jagged–Notch signaling can induce a switch-type behavior in vascular homeostasis Loerakker, Sandra; Stassen, Oscar M. J. A.; Ter Huurne, Fleur M. ETH Zurich https://doi.org/10.3929/ethz-b-000261008	text	January 2018
Comparison of T Cell Activities Mediated by Human TCRs and CARs That Use the Same Recognition Domains Harris, Daniel T.; Hager, Marlies V.; Smith, Sheena N. The Journal of Immunology, Vol. 200, Issue 3 https://doi.org/10.4049/jimmunol.1700236	journal	December 2017
Spatial patterning of liver progenitor cell differentiation mediated by cellular contractility and Notch signaling Kaylan, Kerim B.; Berg, Ian C.; Biehl, Matthew J. eLife, Vol. 7 https://doi.org/10.7554/elife.38536	journal	December 2018
A brighter force gauge for cells Ma, Victor Pui-Yan; Salaita, Khalid eLife, Vol. 7 https://doi.org/10.7554/elife.38959	journal	July 2018
The ectodomains determine ligand function in vivo and selectivity of DLL1 and DLL4 toward NOTCH1 and NOTCH2 in vitro Tveriakhina, Lena; Schuster-Gossler, Karin; Jarrett, Sanchez M. eLife, Vol. 7 https://doi.org/10.7554/elife.40045	journal	October 2018
Missense mutation in SLIT2 associated with congenital myopia, anisometropia, connective tissue abnormalities, and obesity Liu, Katherine Y.; Sengillo, Jesse D.; Velez, Gabriel Columbia University https://doi.org/10.7916/d81c3dqn	text	January 2018

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