Preclinical characterization of Pan-NKG2D ligand-binding NKG2D receptor decoys

Rupert, Peter B.; Buerger, Matthew; Girard, Emily J.; Frutoso, Marie; Parrilla, Don; Ng, Kevin; Gooley, Theodore; Groh, Veronika; Strong, Roland K.

doi:10.1016/j.heliyon.2024.e28583

Title: Preclinical characterization of Pan-NKG2D ligand-binding NKG2D receptor decoys

Journal Article · 26 March 2024 · Heliyon

DOI: https://doi.org/10.1016/j.heliyon.2024.e28583 · OSTI ID:2471028

Rupert, Peter B. ^[1]; Buerger, Matthew ^[1]; Girard, Emily J. ^[2]; Frutoso, Marie ^[2]; Parrilla, Don ^[2]; Ng, Kevin ^[1]; Gooley, Theodore ^[1]; Groh, Veronika ^[1];

^[1]

Fred Hutchinson Cancer Center, Seattle, WA (United States)
Fred Hutchinson Cancer Center, Seattle, WA (United States); Seattle Children's Research Institute, Renton, WA (United States)

NKG2D and its ligands are critical regulators of protective immune responses controlling infections and cancer, defining a crucial immune signaling axis. Current therapeutic efforts targeting this axis almost exclusively aim at enhancing NKG2D-mediated effector functions. However, this axis can drive disease processes when dysregulated, in particular, driving stem-like cancer cell reprogramming and tumorigenesis through receptor/ligand self-stimulation on tumor cells. Despite complexities with its structure and biology, we developed multiple novel engineered proteins that functionally serve as axis-blocking NKG2D “decoys” and report biochemical, structural, in vitro, and in vivo evaluation of their functionality.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Sponsoring Organization:: National Cancer Institute (NCI); National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2471028

Journal Information:: Heliyon, Journal Name: Heliyon Journal Issue: 7 Vol. 10; ISSN 2405-8440

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

An Fc‐optimized NKG2D‐immunoglobulin G fusion protein for induction of natural killer cell reactivity against leukemia Steinbacher, Julia; Baltz‐Ghahremanpour, Katrin; Schmiedel, Benjamin Joachim International Journal of Cancer, Vol. 136, Issue 5 https://doi.org/10.1002/ijc.29083	journal	July 2014
NKG2D-Fc fusion protein promotes antitumor immunity through the depletion of immunosuppressive cells Feng, Po-Hao; Lam, Brandon; Tseng, Ssu-Hsueh Cancer Immunology, Immunotherapy, Vol. 69, Issue 10 https://doi.org/10.1007/s00262-020-02615-7	journal	May 2020
Labeling of proteins by reductive methylation using sodium cyanoborohydride. Jentoft, N.; Dearborn, D. G. Journal of Biological Chemistry, Vol. 254, Issue 11 https://doi.org/10.1016/S0021-9258(17)30016-9	journal	June 1979
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Symmetry Recognizing Asymmetry McFarland, Benjamin J.; Kortemme, Tanja; Yu, Shuyuarn F. Structure, Vol. 11, Issue 4 https://doi.org/10.1016/S0969-2126(03)00047-9	journal	April 2003
Crystal Structure of the MHC Class I Homolog MIC-A, a γδ T Cell Ligand Li, Pingwei; Willie, Sirkku T.; Bauer, Stefan Immunity, Vol. 10, Issue 5 https://doi.org/10.1016/S1074-7613(00)80057-6	journal	May 1999
Conformational Plasticity Revealed by the Cocrystal Structure of NKG2D and Its Class I MHC-like Ligand ULBP3 Radaev, Sergei; Rostro, Bertha; Brooks, Andrew G. Immunity, Vol. 15, Issue 6 https://doi.org/10.1016/S1074-7613(01)00241-2	journal	December 2001
Thermodynamic Analysis of Degenerate Recognition by the NKG2D Immunoreceptor McFarland, Benjamin J.; Strong, Roland K. Immunity, Vol. 19, Issue 6 https://doi.org/10.1016/S1074-7613(03)00320-0	journal	December 2003
Lipocalin-2: Structure, function, distribution and role in metabolic disorders Jaberi, Saeeda Al; Cohen, Athena; D’Souza, Crystal Biomedicine & Pharmacotherapy, Vol. 142 https://doi.org/10.1016/j.biopha.2021.112002	journal	October 2021
Immune Surveillance and Therapy of Lymphomas Driven by Epstein-Barr Virus Protein LMP1 in a Mouse Model Zhang, Baochun; Kracker, Sven; Yasuda, Tomoharu Cell, Vol. 148, Issue 4 https://doi.org/10.1016/j.cell.2011.12.031	journal	February 2012
PKSolver: An add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel Zhang, Yong; Huo, Meirong; Zhou, Jianping Computer Methods and Programs in Biomedicine, Vol. 99, Issue 3 https://doi.org/10.1016/j.cmpb.2010.01.007	journal	September 2010
Coordinated Induction by IL15 of a TCR-Independent NKG2D Signaling Pathway Converts CTL into Lymphokine-Activated Killer Cells in Celiac Disease Meresse, Bertrand; Chen, Zhangguo; Ciszewski, Cezary Immunity, Vol. 21, Issue 3 https://doi.org/10.1016/j.immuni.2004.06.020	journal	September 2004
NKG2D ligands: key targets of the immune response González, Segundo; López-Soto, Alejandro; Suarez-Alvarez, Beatriz Trends in Immunology, Vol. 29, Issue 8 https://doi.org/10.1016/j.it.2008.04.007	journal	August 2008
Tobacco Etch Virus protease: A shortcut across biotechnologies Cesaratto, Francesca; Burrone, Oscar R.; Petris, Gianluca Journal of Biotechnology, Vol. 231 https://doi.org/10.1016/j.jbiotec.2016.06.012	journal	August 2016
A TfR-Binding Cystine-Dense Peptide Promotes Blood–Brain Barrier Penetration of Bioactive Molecules Crook, Zachary R.; Girard, Emily; Sevilla, Gregory P. Journal of Molecular Biology, Vol. 432, Issue 14 https://doi.org/10.1016/j.jmb.2020.04.002	journal	June 2020
Control of Tumor Initiation by NKG2D Naturally Expressed on Ovarian Cancer Cells Cai, Xin; Caballero-Benitez, Andrea; Gewe, Mesfin M. Neoplasia, Vol. 19, Issue 6 https://doi.org/10.1016/j.neo.2017.03.005	journal	June 2017
NKG2D-mediated activation of cytotoxic lymphocytes: Unique signaling pathways and distinct functional outcomes Upshaw, Jadee L.; Leibson, Paul J. Seminars in Immunology, Vol. 18, Issue 3 https://doi.org/10.1016/j.smim.2006.03.001	journal	June 2006
Glycoprotein Structural Genomics: Solving the Glycosylation Problem Chang, Veronica T.; Crispin, Max; Aricescu, A. Radu Structure, Vol. 15, Issue 3 https://doi.org/10.1016/j.str.2007.01.011	journal	March 2007
Complex structure of the activating immunoreceptor NKG2D and its MHC class I–like ligand MICA Li, Pingwei; Morris, Daniel L.; Willcox, Benjamin E. Nature Immunology, Vol. 2, Issue 5 https://doi.org/10.1038/87757	journal	May 2001
Genome-wide association study in alopecia areata implicates both innate and adaptive immunity Petukhova, Lynn; Duvic, Madeleine; Hordinsky, Maria Nature, Vol. 466, Issue 7302 https://doi.org/10.1038/nature09114	journal	July 2010
Fas ligand–mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity Groh, Veronika; Smythe, Kimberly; Dai, Zhenpeng Nature Immunology, Vol. 7, Issue 7 https://doi.org/10.1038/ni1350	journal	May 2006
Promiscuity and the single receptor: NKG2D Eagle, Robert A.; Trowsdale, John Nature Reviews Immunology, Vol. 7, Issue 9 https://doi.org/10.1038/nri2144	journal	August 2007
Effects on tumor development and metastatic dissemination by the NKG2D lymphocyte receptor expressed on cancer cells El-Gazzar, A.; Cai, X.; Reeves, R. S. Oncogene, Vol. 33, Issue 41 https://doi.org/10.1038/onc.2013.435	journal	October 2013
Severe COVID-19 patients exhibit an ILC2 NKG2D+ population in their impaired ILC compartment Gomez-Cadena, Alejandra; Spehner, Laurie; Kroemer, Marie Cellular & Molecular Immunology, Vol. 18, Issue 2 https://doi.org/10.1038/s41423-020-00596-2	journal	December 2020
CD4+NKG2D+ T Cells in Crohn’s Disease Mediate Inflammatory and Cytotoxic Responses Through MICA Interactions Allez, Matthieu; Tieng, Vannary; Nakazawa, Atsushi Gastroenterology, Vol. 132, Issue 7 https://doi.org/10.1053/j.gastro.2007.03.025	journal	June 2007
The activating NKG2D receptor assembles in the membrane with two signaling dimers into a hexameric structure Garrity, David; Call, Matthew E.; Feng, Jianwen Proceedings of the National Academy of Sciences, Vol. 102, Issue 21 https://doi.org/10.1073/pnas.0502439102	journal	May 2005
Expression, signaling proficiency, and stimulatory function of the NKG2D lymphocyte receptor in human cancer cells Benitez, Andrea Caballero; Dai, Zhenpeng; Mann, Henning H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 10 https://doi.org/10.1073/pnas.1018603108	journal	February 2011
Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis Groh, Veronika; Brühl, Anja; El-Gabalawy, Hani Proceedings of the National Academy of Sciences, Vol. 100, Issue 16 https://doi.org/10.1073/pnas.1632807100	journal	July 2003
Mutations Designed to Destabilize the Receptor-Bound Conformation Increase MICA-NKG2D Association Rate and Affinity Lengyel, Candice S. E.; Willis, Lindsey J.; Mann, Patrick Journal of Biological Chemistry, Vol. 282, Issue 42 https://doi.org/10.1074/jbc.M704513200	journal	October 2007
Affinity of human IgG subclasses to mouse Fc gamma receptors Dekkers, Gillian; Bentlage, Arthur E. H.; Stegmann, Tamara C. mAbs, Vol. 9, Issue 5 https://doi.org/10.1080/19420862.2017.1323159	journal	May 2017
Engaging natural killer cells for cancer therapy via NKG2D, CD16A and other receptors Whalen, Kerry A.; Rakhra, Kavya; Mehta, Naveen K. mAbs, Vol. 15, Issue 1 https://doi.org/10.1080/19420862.2023.2208697	journal	May 2023
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
Daedalus: a robust, turnkey platform for rapid production of decigram quantities of active recombinant proteins in human cell lines using novel lentiviral vectors Bandaranayake, Ashok D.; Correnti, Colin; Ryu, Byoung Y. Nucleic Acids Research, Vol. 39, Issue 21 https://doi.org/10.1093/nar/gkr706	journal	September 2011
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
A graphical user interface to the CCP 4 program suite Potterton, Elizabeth; Briggs, Peter; Turkenburg, Maria Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7 https://doi.org/10.1107/S0907444903008126	journal	June 2003
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042589	journal	December 2009
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
Activation of NK Cells and T Cells by NKG2D, a Receptor for Stress-Inducible MICA Bauer, S. Science, Vol. 285, Issue 5428 https://doi.org/10.1126/science.285.5428.727	journal	July 1999
An Activating Immunoreceptor Complex Formed by NKG2D and DAP10 Wu, Jun; Song, Yaoli; Bakker, Alexander B. H. Science, Vol. 285, Issue 5428 https://doi.org/10.1126/science.285.5428.730	journal	July 1999
A disease-linked ULBP6 polymorphism inhibits NKG2D-mediated target cell killing by enhancing the stability of NKG2D ligand binding Zuo, Jianmin; Willcox, Carrie R.; Mohammed, Fiyaz Science Signaling, Vol. 10, Issue 481 https://doi.org/10.1126/scisignal.aai8904	journal	May 2017
Anti-NKG2D monoclonal antibody (NNC0142-0002) in active Crohn's disease: a randomised controlled trial Allez, Matthieu; Skolnick, Brett E.; Wisniewska-Jarosinska, Maria Gut, Vol. 66, Issue 11 https://doi.org/10.1136/gutjnl-2016-311824	journal	August 2016
Regulation of Ligands for the NKG2D Activating Receptor Raulet, David H.; Gasser, Stephan; Gowen, Benjamin G. Annual Review of Immunology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev-immunol-032712-095951	journal	March 2013
NKG2D Receptor and Its Ligands in Host Defense Lanier, Lewis L. Cancer Immunology Research, Vol. 3, Issue 6 https://doi.org/10.1158/2326-6066.CIR-15-0098	journal	June 2015
Arming oHSV with ULBP3 drives abscopal immunity in lymphocyte-depleted glioblastoma Wirsching, Hans-Georg; Zhang, Huajia; Szulzewsky, Frank JCI Insight, Vol. 4, Issue 13 https://doi.org/10.1172/jci.insight.128217	journal	July 2019
Autonomous Stimulation of Cancer Cell Plasticity by the Human NKG2D Lymphocyte Receptor Coexpressed with Its Ligands on Cancer Cells Cai, Xin; Dai, Zhenpeng; Reeves, Rebecca S. PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0108942	journal	October 2014
MICA and NKG2D: Is There an Impact on Kidney Transplant Outcome? Risti, Matilde; Bicalho, Maria da Graça Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.00179	journal	February 2017
The Role of Natural Killer Group 2, Member D in Chronic Inflammation and Autoimmunity Babic, Marina; Romagnani, Chiara Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.01219	journal	May 2018
The Paradoxical Role of NKG2D in Cancer Immunity Sheppard, Sam; Ferry, Amir; Guedes, Joana Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.01808	journal	August 2018
Overcoming Target Driven Fratricide for T Cell Therapy Breman, Eytan; Demoulin, Benjamin; Agaugué, Sophie Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.02940	journal	December 2018
Fc-Optimized NKG2D–Fc Constructs Induce NK Cell Antibody-Dependent Cellular Cytotoxicity against Breast Cancer Cells Independently of HER2/neu Expression Status Raab, Stefanie; Steinbacher, Julia; Schmiedel, Benjamin J. The Journal of Immunology, Vol. 193, Issue 8 https://doi.org/10.4049/jimmunol.1400872	journal	October 2014

Similar Records

Identification of small-molecule protein–protein interaction inhibitors for NKG2D

Journal Article · 2023 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:2423465

Thompson, Aaron A.; Harbut, Michael B.; Kung, Pei-Pei; +37 more

The HHV-6B U20 glycoprotein binds ULBP1, masking it from recognition by NKG2D and interfering with natural killer cell activation

Journal Article · 2024 · Frontiers in Immunology · OSTI ID:2470306

Weaver, Grant C.; Schneider, Christine L.; Becerra-Artiles, Aniuska; +3 more

Parallel Evolution of Chemokine Binding by Structurally Related Herpesvirus Decoy Receptors

Journal Article · 2015 · Structure · OSTI ID:1237760

Lubman, Olga Y.; Fremont, Daved H.

Related Subjects

60 APPLIED LIFE SCIENCES
Engineered biologic immunotherapeutics
NKG2D
Natural killer cell receptors
X-ray crystallography

Title: Preclinical characterization of Pan-NKG2D ligand-binding NKG2D receptor decoys

Citation Formats

References (54)

Similar Records

Related Subjects