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

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1360203

Alternate ID(s):: OSTI ID: 1353229

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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Missense mutation in SLIT2 associated with congenital myopia, anisometropia, connective tissue abnormalities, and obesity Liu, Katherine Y.; Sengillo, Jesse D.; Velez, Gabriel Orphanet Journal of Rare Diseases, Vol. 13, Issue 1 https://doi.org/10.1186/s13023-018-0885-4	journal	August 2018
Tensile and compressive force regulation on cell mechanosensing Chen, Yunfeng; Li, Zhiyong; Ju, Lining Arnold Biophysical Reviews, Vol. 11, Issue 3 https://doi.org/10.1007/s12551-019-00536-z	journal	May 2019
Mechanosensing through immunoreceptors Zhu, Cheng; Chen, Wei; Lou, Jizhong Nature Immunology, Vol. 20, Issue 10 https://doi.org/10.1038/s41590-019-0491-1	journal	September 2019
DLK proteins modulate NOTCH signaling to influence a brown or white 3T3-L1 adipocyte fate Nueda, María-Luisa; González-Gómez, María-Julia; Rodríguez-Cano, María-Milagros Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35252-3	journal	November 2018
The Molecular Mechanism of Notch Activation Lovendahl, Klaus N.; Blacklow, Stephen C.; Gordon, Wendy R. Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-3-319-89512-3_3	book	January 2018
DNA Nanotechnology as an Emerging Tool to Study Mechanotransduction in Living Systems Ma, Victor Pui‐Yan; Salaita, Khalid Small, Vol. 15, Issue 26 https://doi.org/10.1002/smll.201900961	journal	February 2019
Notch Signaling in Development, Tissue Homeostasis, and Disease Siebel, Chris; Lendahl, Urban Physiological Reviews, Vol. 97, Issue 4 https://doi.org/10.1152/physrev.00005.2017	journal	October 2017
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
Force transduction by cadherin adhesions in morphogenesis Pannekoek, Willem-Jan; de Rooij, Johan; Gloerich, Martijn F1000Research, Vol. 8 https://doi.org/10.12688/f1000research.18779.1	journal	January 2019
A modifier in the 129S2/SvPasCrl genome is responsible for the viability of Notch1[12f/12f] mice Varshney, Shweta; Wei, Hua-Xing; Batista, Frank BMC Developmental Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12861-019-0199-3	journal	October 2019
Effects of Notch glycosylation on health and diseases Urata, Yusuke; Takeuchi, Hideyuki Development, Growth & Differentiation, Vol. 62, Issue 1 https://doi.org/10.1111/dgd.12643	journal	December 2019

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