TY - JOUR
T1 - GPR120 signaling controls amyloid-b degrading activity of matrix metalloproteinases
AU - Kikuchi, Kazunori
AU - Tatebe, Takuya
AU - Sudo, Yuki
AU - Yokoyama, Miyabishara
AU - Kidana, Kiwami
AU - Chiu, Yung Wen
AU - Takatori, Sho
AU - Arita, Makoto
AU - Hori, Yukiko
AU - Tomita, Taisuke
N1 - Funding Information:
This work was supported by Japan Society for the Promotion of Science Grants-in-aid for Scientific Research (A) 15H02492 and 19H01015 to T. Tomita; and Japan Agency for Medical Research and Development Strategic Research Program for Brain Sciences 19dm0107056h0004 to T. Tomita. The results of the MayoRNAseq Study and Mount Sinai Brain Bank data were published in whole or in part based on data obtained from the AMP-AD Knowledge Portal (https://adknowledgeportal.synapse.org/). The MayoRNAseq Study data were provided by the following sources: Mayo Clinic Alzheimer’s Disease Genetic Studies, led by Dr. Nilufer Taner and Dr. Steven G. Younkin (Mayo Clinic, Jacksonville, FL) using samples from the Mayo Clinic Study of Aging, the Mayo Clinic Alzheimer’s Disease Research Center, and the Mayo Clinic Brain Bank. Data collection was supported through funding by National Institute on Aging Grants P50 AG016574, R01 AG032990, U01 AG046139, R01 AG018023, U01 AG006576, U01 AG006786, R01 AG025711, R01 AG017216, and R01 AG003949; National Institute of Neurological Disorders and Stroke Grant R01 NS080820; CurePSP Foundation; and Mayo Foundation. Study data include samples collected through the Sun Health Research Institute Brain and Body Donation Program (Sun City, AZ). The Brain and Body Donation Program was supported by National Institute of Neurological Disorders and Stroke (U24 NS072026 National Brain and Tissue Resource for Parkinson’s Disease and Related Disorders), National Institute on Aging (P30 AG19610 Arizona Alzheimer’s Disease Core Center), Arizona Department of Health Services (Contract 211002, Arizona Alzheimer’s Research Center), Arizona Biomedical Research Commission (Contracts 4001, 0011, 05-901, and 1001 to the Arizona Parkinson’s Disease Consortium), and Michael J. Fox Foundation for Parkinson’s Research. The Mount Sinai Brain Bank data were generated from postmortem brain tissue collected through the Mount Sinai Veterans Administration Medical Center Brain Bank and were provided by Dr. Eric Schadt (Mount Sinai School of Medicine). We thank Drs. Takeshi Iwatsubo (The University of Tokyo) for APP/PS1 mice; Haruhiko Bito (The University of Tokyo) for lentivirus vectors; Edward Koo (University of California, San Diego) for 7PA2 cells; Keisuke Horiuchi and Yasunori Okada (Keio University) for mouse sample; Hideki Kitaura and Itaru Mizoguchi (Tohoku University) for mouse sample; Atsuhiko Ichimura (Kyoto University) for mouse sample; and current and previous laboratory members for helpful discussions.
Funding Information:
This work was supported by Japan Society for the Promotion of Science Grants-in-aid for Scientific Research (A) 15H02492 and 19H01015 to T. Tomita; and Japan Agency for Medical Research and Development Strategic Research Program for Brain Sciences 19dm0107056h0004 to T. Tomita. The results of the MayoRNAseq Study and Mount Sinai Brain Bank data were published in whole or in part based on data obtained from the AMP-AD Knowledge Portal (https://adknowledgeportal.synapse.org/). The MayoRNAseq Study data were provided by the following sources: Mayo Clinic Alzheimer’s Disease Genetic Studies, led by Dr. Nilufer Taner and Dr. Steven G. Younkin (Mayo Clinic, Jacksonville, FL) using samples from the Mayo Clinic Study of Aging, the Mayo Clinic Alzheimer’s Disease Research Center, and the Mayo Clinic Brain Bank. Data collection was supported through funding by National Institute on Aging Grants P50 AG016574, R01 AG032990, U01 AG046139, R01 AG018023, U01 AG006576, U01 AG006786, R01 AG025711, R01 AG017216, and R01 AG003949; National Institute of Neurological Disorders and Stroke Grant R01 NS080820; CurePSP Foundation; and Mayo Foundation. Study data include samples collected through the Sun Health Research Institute Brain and Body Donation Program (Sun City, AZ). The Brain and Body Donation Program was supported by National Institute of Neurological Disorders and Stroke (U24 NS072026 National Brain and Tissue Resource for Parkinson’s Disease and Related Disorders), National Institute on Aging (P30 AG19610 Arizona Alzheimer’s Disease Core Center), Arizona Department of Health Services (Contract 211002, Arizona Alzheimer’s Research Center), Arizona Biomedical Research Commission (Contracts 4001, 0011, 05-901, and 1001 to the Arizona Parkinson’s Disease Consortium), and Michael J. Fox Foundation for Parkinson’s Research. The Mount Sinai Brain Bank data were generated from postmortem brain tissue collected through the Mount Sinai Veterans Administration Medical Center Brain Bank and were provided by Dr. Eric Schadt (Mount Sinai School of Medicine). We thank Drs. Takeshi Iwatsubo (The University of Tokyo) for APP/PS1 mice; Haruhiko Bito (The University of Tokyo) for lentivirus vectors; Edward Koo (University of California, San Diego) for 7PA2 cells; Keisuke Horiuchi and Yasunori Okada (Keio University) for mouse sample; Hideki Kitaura and Itaru Mizoguchi (Tohoku University) for mouse sample; Atsuhiko Ichimura (Kyoto University) for mouse sample; and current and previous laboratory members for helpful discussions. The authors declare no competing financial interests. Correspondence should be addressed to Taisuke Tomita at taisuke@mol.f.u-tokyo.ac.jp. https://doi.org/10.1523/JNEUROSCI.2595-20.2021 Copyright © 2021 the authors
Publisher Copyright:
Copyright © 2021 the authors.
PY - 2021/7/14
Y1 - 2021/7/14
N2 - Alzheimer’s disease (AD) is characterized by the extensive deposition of amyloid-b peptide (Ab) in the brain. Brain Ab level is regulated by a balance between Ab production and clearance. The clearance rate of Ab is decreased in the brains of sporadic AD patients, indicating that the dysregulation of Ab clearance mechanisms affects the pathologic process of AD. Astrocytes are among the most abundant cells in the brain and are implicated in the clearance of brain Ab via their regulation of the blood–brain barrier, glymphatic system, and proteolytic degradation. The cellular morphology and activity of astrocytes are modulated by several molecules, including x3 polyunsaturated fatty acids, such as docosahexaenoic acid, which is one of the most abundant lipids in the brain, via the G protein-coupled receptor GPR120/FFAR4. In this study, we analyzed the role of GPR120 signaling in the Ab-degrading activity of astrocytes. Treatment with the selective antagonist upregulated the matrix metalloproteinase (MMP) inhibitor-sensitive Ab-degrading activity in primary astrocytes. Moreover, the inhibition of GPR120 signaling increased the levels of Mmp2 and Mmp14 mRNAs, and decreased the expression levels of tissue inhibitor of metalloproteinases 3 (Timp3) and Timp4, suggesting that GPR120 negatively regulates the astrocyte-derived MMP network. Finally, the intracerebral injection of GPR120-specific antagonist substantially decreased the levels of TBS-soluble Ab in male AD model mice, and this effect was canceled by the coinjection of an MMP inhibitor. These data indicate that astrocytic GPR120 signaling negatively regulates the Ab-degrading activity of MMPs.
AB - Alzheimer’s disease (AD) is characterized by the extensive deposition of amyloid-b peptide (Ab) in the brain. Brain Ab level is regulated by a balance between Ab production and clearance. The clearance rate of Ab is decreased in the brains of sporadic AD patients, indicating that the dysregulation of Ab clearance mechanisms affects the pathologic process of AD. Astrocytes are among the most abundant cells in the brain and are implicated in the clearance of brain Ab via their regulation of the blood–brain barrier, glymphatic system, and proteolytic degradation. The cellular morphology and activity of astrocytes are modulated by several molecules, including x3 polyunsaturated fatty acids, such as docosahexaenoic acid, which is one of the most abundant lipids in the brain, via the G protein-coupled receptor GPR120/FFAR4. In this study, we analyzed the role of GPR120 signaling in the Ab-degrading activity of astrocytes. Treatment with the selective antagonist upregulated the matrix metalloproteinase (MMP) inhibitor-sensitive Ab-degrading activity in primary astrocytes. Moreover, the inhibition of GPR120 signaling increased the levels of Mmp2 and Mmp14 mRNAs, and decreased the expression levels of tissue inhibitor of metalloproteinases 3 (Timp3) and Timp4, suggesting that GPR120 negatively regulates the astrocyte-derived MMP network. Finally, the intracerebral injection of GPR120-specific antagonist substantially decreased the levels of TBS-soluble Ab in male AD model mice, and this effect was canceled by the coinjection of an MMP inhibitor. These data indicate that astrocytic GPR120 signaling negatively regulates the Ab-degrading activity of MMPs.
KW - Alzheimer
KW - Amyloid-beta
KW - Astrocyte
KW - Degradation
KW - Matrix metalloproteinase
KW - Protease
UR - http://www.scopus.com/inward/record.url?scp=85111550856&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85111550856&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.2595-20.2021
DO - 10.1523/JNEUROSCI.2595-20.2021
M3 - Article
C2 - 34099509
AN - SCOPUS:85111550856
SN - 0270-6474
VL - 41
SP - 6173
EP - 6185
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 28
ER -