A split-luciferase complementation, real-time reporting assay enables monitoring of the disease-associated transmembrane protein TREM2 in live cells

Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically linked to Nasu-Hakola disease and associated with multiple neurodegenerative disorders, including Alzheimer's disease. TREM2 may regulate...

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Published inThe Journal of biological chemistry Vol. 292; no. 25; pp. 10651 - 10663
Main Authors Varnum, Megan M., Clayton, Kevin A., Yoshii-Kitahara, Asuka, Yonemoto, Grant, Koro, Lacin, Ikezu, Seiko, Ikezu, Tsuneya
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.06.2017
American Society for Biochemistry and Molecular Biology
Subjects
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Alzheimer disease
Alzheimer Disease - genetics
Alzheimer Disease - metabolism
Alzheimer's disease
Animals
cell culture
Cell Line
Flow Cytometry - methods
Genetic Complementation Test - methods
genetic polymorphism
Humans
Lipodystrophy - genetics
Lipodystrophy - metabolism
Luciferases, Renilla - metabolism
Membrane Glycoproteins - genetics
Membrane Glycoproteins - metabolism
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mice
microglia
Microglia - metabolism
Molecular Bases of Disease
Osteochondrodysplasias - genetics
Osteochondrodysplasias - metabolism
phagocytosis
plasmid
Receptors, Immunologic - genetics
Receptors, Immunologic - metabolism
Subacute Sclerosing Panencephalitis - genetics
Subacute Sclerosing Panencephalitis - metabolism
Syk Kinase - genetics
Syk Kinase - metabolism
phagocytosis
Alzheimer disease
cell culture
plasmid
genetic polymorphism
microglia
Alzheimer's disease
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Abstract Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically linked to Nasu-Hakola disease and associated with multiple neurodegenerative disorders, including Alzheimer's disease. TREM2 may regulate microglial inflammation and phagocytosis through coupling to the adaptor protein TYRO protein-tyrosine kinase-binding protein (TYROBP). However, there is no functional system for monitoring this protein-protein interaction. We developed a luciferase-based modality for real-time monitoring of TREM2-TYROBP coupling in live cells that utilizes split-luciferase complementation technology based on TREM2 and TYROBP fusion to the C- or N-terminal portion of the Renilla luciferase gene. Transient transfection of human embryonic kidney 293 cells with this reporter vector increased luciferase activity upon stimulation with an anti-TREM2 antibody, which induces their homodimerization. This was confirmed by ELISA-based analysis of the TREM2-TYROBP interaction. Antibody-mediated TREM2 stimulation enhanced spleen tyrosine kinase (SYK) activity and uptake of Staphylococcus aureus in microglial cell line BV-2 in a kinase-dependent manner. Interestingly, the TREM2 T66M mutation significantly enhanced luciferase activity without stimulation, indicating constitutive coupling to TYROBP. Finally, flow cytometry analyses indicated significantly lower surface expression of T66M TREM2 variant than wild type or other TREM2 variants. These results demonstrate that our TREM2 reporter vector is a novel tool for monitoring the TREM2-TYROBP interaction in real time.
AbstractList Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically linked to Nasu-Hakola disease and associated with multiple neurodegenerative disorders, including Alzheimer's disease. TREM2 may regulate microglial inflammation and phagocytosis through coupling to the adaptor protein TYRO protein-tyrosine kinase-binding protein (TYROBP). However, there is no functional system for monitoring this protein-protein interaction. We developed a luciferase-based modality for real-time monitoring of TREM2-TYROBP coupling in live cells that utilizes split-luciferase complementation technology based on TREM2 and TYROBP fusion to the C- or N-terminal portion of the luciferase gene. Transient transfection of human embryonic kidney 293 cells with this reporter vector increased luciferase activity upon stimulation with an anti-TREM2 antibody, which induces their homodimerization. This was confirmed by ELISA-based analysis of the TREM2-TYROBP interaction. Antibody-mediated TREM2 stimulation enhanced spleen tyrosine kinase (SYK) activity and uptake of in microglial cell line BV-2 in a kinase-dependent manner. Interestingly, the TREM2 T66M mutation significantly enhanced luciferase activity without stimulation, indicating constitutive coupling to TYROBP. Finally, flow cytometry analyses indicated significantly lower surface expression of T66M TREM2 variant than wild type or other TREM2 variants. These results demonstrate that our TREM2 reporter vector is a novel tool for monitoring the TREM2-TYROBP interaction in real time.
Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically linked to Nasu-Hakola disease and associated with multiple neurodegenerative disorders, including Alzheimer's disease. TREM2 may regulate microglial inflammation and phagocytosis through coupling to the adaptor protein TYRO protein-tyrosine kinase-binding protein (TYROBP). However, there is no functional system for monitoring this protein-protein interaction. We developed a luciferase-based modality for real-time monitoring of TREM2-TYROBP coupling in live cells that utilizes split-luciferase complementation technology based on TREM2 and TYROBP fusion to the C- or N-terminal portion of the Renilla luciferase gene. Transient transfection of human embryonic kidney 293 cells with this reporter vector increased luciferase activity upon stimulation with an anti-TREM2 antibody, which induces their homodimerization. This was confirmed by ELISA-based analysis of the TREM2-TYROBP interaction. Antibody-mediated TREM2 stimulation enhanced spleen tyrosine kinase (SYK) activity and uptake of Staphylococcus aureus in microglial cell line BV-2 in a kinase-dependent manner. Interestingly, the TREM2 T66M mutation significantly enhanced luciferase activity without stimulation, indicating constitutive coupling to TYROBP. Finally, flow cytometry analyses indicated significantly lower surface expression of T66M TREM2 variant than wild type or other TREM2 variants. These results demonstrate that our TREM2 reporter vector is a novel tool for monitoring the TREM2-TYROBP interaction in real time.
Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically linked to Nasu-Hakola disease and associated with multiple neurodegenerative disorders, including Alzheimer's disease. TREM2 may regulate microglial inflammation and phagocytosis through coupling to the adaptor protein TYRO protein-tyrosine kinase-binding protein (TYROBP). However, there is no functional system for monitoring this protein-protein interaction. We developed a luciferase-based modality for real-time monitoring of TREM2-TYROBP coupling in live cells that utilizes split-luciferase complementation technology based on TREM2 and TYROBP fusion to the C- or N-terminal portion of the Renilla luciferase gene. Transient transfection of human embryonic kidney 293 cells with this reporter vector increased luciferase activity upon stimulation with an anti-TREM2 antibody, which induces their homodimerization. This was confirmed by ELISA-based analysis of the TREM2-TYROBP interaction. Antibody-mediated TREM2 stimulation enhanced spleen tyrosine kinase (SYK) activity and uptake of Staphylococcus aureus in microglial cell line BV-2 in a kinase-dependent manner. Interestingly, the TREM2 T66M mutation significantly enhanced luciferase activity without stimulation, indicating constitutive coupling to TYROBP. Finally, flow cytometry analyses indicated significantly lower surface expression of T66M TREM2 variant than wild type or other TREM2 variants. These results demonstrate that our TREM2 reporter vector is a novel tool for monitoring the TREM2-TYROBP interaction in real time.
Author Koro, Lacin
Clayton, Kevin A.
Yonemoto, Grant
Ikezu, Seiko
Varnum, Megan M.
Yoshii-Kitahara, Asuka
Ikezu, Tsuneya
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  email: tikezu@bu.edu
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Copyright 2017 © 2017 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.
2017 by The American Society for Biochemistry and Molecular Biology, Inc.
2017 by The American Society for Biochemistry and Molecular Biology, Inc. 2017 The American Society for Biochemistry and Molecular Biology, Inc.
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Issue 25
Keywords phagocytosis
Alzheimer disease
cell culture
plasmid
genetic polymorphism
microglia
Alzheimer's disease
Language English
License This is an open access article under the CC BY license.
2017 by The American Society for Biochemistry and Molecular Biology, Inc.
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Snippet Triggering receptor expressed on myeloid cells 2 (TREM2) is a single transmembrane molecule uniquely expressed in microglia. TREM2 mutations are genetically...
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SubjectTerms Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Alzheimer disease
Alzheimer Disease - genetics
Alzheimer Disease - metabolism
Alzheimer's disease
Animals
cell culture
Cell Line
Flow Cytometry - methods
Genetic Complementation Test - methods
genetic polymorphism
Humans
Lipodystrophy - genetics
Lipodystrophy - metabolism
Luciferases, Renilla - metabolism
Membrane Glycoproteins - genetics
Membrane Glycoproteins - metabolism
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mice
microglia
Microglia - metabolism
Molecular Bases of Disease
Osteochondrodysplasias - genetics
Osteochondrodysplasias - metabolism
phagocytosis
plasmid
Receptors, Immunologic - genetics
Receptors, Immunologic - metabolism
Subacute Sclerosing Panencephalitis - genetics
Subacute Sclerosing Panencephalitis - metabolism
Syk Kinase - genetics
Syk Kinase - metabolism
Title A split-luciferase complementation, real-time reporting assay enables monitoring of the disease-associated transmembrane protein TREM2 in live cells
URI https://dx.doi.org/10.1074/jbc.M116.759159
https://www.ncbi.nlm.nih.gov/pubmed/28490631
https://search.proquest.com/docview/1897806326
https://pubmed.ncbi.nlm.nih.gov/PMC5481570
Volume 292
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