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Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases
Erik Nutma 
,
Nurun Fancy ,
Maria Weinert ,
Stergios Tsartsalis ,
Manuel C. Marzin,
Robert C. J. Muirhead,
Irene Falk,
Marjolein Breur,
Joy de Bruin,
David Hollaus,
Robin Pieterman,
Jasper Anink,
David Story,
Siddharthan Chandran,
Jiabin Tang,
Maria C. Trolese ,
Takashi Saito ,
Takaomi C. Saido,
Katharine H. Wiltshire,
Paula Beltran-Lobo,
Alexandra Phillips,
Jack Antel ,
Luke Healy ,
Marie-France Dorion,
Dylan A. Galloway,
Rochelle Y. Benoit,
Quentin Amossé ,
Kelly Ceyzériat,
Aurélien M. Badina ,
Enikö Kövari,
Caterina Bendotti ,
Eleonora Aronica ,
Carola I. Radulescu,
Jia Hui Wong ,
Anna M. Barron ,
Amy M. Smith,
Samuel J. Barnes ,
David W. Hampton,
Paul van der Valk,
Steven Jacobson,
Owain Howell ,
David Baker,
Markus Kipp ,
Hannes Kaddatz ,
Benjamin B. Tournier ,
Philippe Millet ,
Paul M. Matthews ,
Craig S. Moore ,
Sandra Amor,
David R. Owen
,
Nurun Fancy ,
Maria Weinert ,
Stergios Tsartsalis ,
Manuel C. Marzin,
Robert C. J. Muirhead,
Irene Falk,
Marjolein Breur,
Joy de Bruin,
David Hollaus,
Robin Pieterman,
Jasper Anink,
David Story,
Siddharthan Chandran,
Jiabin Tang,
Maria C. Trolese ,
Takashi Saito ,
Takaomi C. Saido,
Katharine H. Wiltshire,
Paula Beltran-Lobo,
Alexandra Phillips,
Jack Antel ,
Luke Healy ,
Marie-France Dorion,
Dylan A. Galloway,
Rochelle Y. Benoit,
Quentin Amossé ,
Kelly Ceyzériat,
Aurélien M. Badina ,
Enikö Kövari,
Caterina Bendotti ,
Eleonora Aronica ,
Carola I. Radulescu,
Jia Hui Wong ,
Anna M. Barron ,
Amy M. Smith,
Samuel J. Barnes ,
David W. Hampton,
Paul van der Valk,
Steven Jacobson,
Owain Howell ,
David Baker,
Markus Kipp ,
Hannes Kaddatz ,
Benjamin B. Tournier ,
Philippe Millet ,
Paul M. Matthews ,
Craig S. Moore ,
Sandra Amor,
David R. Owen
Nature Communications, Volume: 14, Issue: 1
Swansea University Author:
Owain Howell
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DOI (Published version): 10.1038/s41467-023-40937-z
Abstract
Microglial activation plays central roles in neuroinflammatory and neurodegenerative diseases. Positron emission tomography (PET) targeting 18 kDa Translocator Protein (TSPO) is widely used for localising inflammation in vivo, but its quantitative interpretation remains uncertain. We show that TSPO...
| Published in: | Nature Communications |
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| ISSN: | 2041-1723 |
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Springer Science and Business Media LLC
2023
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<?xml version="1.0" encoding="utf-8"?><rfc1807 xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xmlns:xsd="http://www.w3.org/2001/XMLSchema"><bib-version>v2</bib-version><id>64510</id><entry>2023-09-12</entry><title>Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases</title><swanseaauthors><author><sid>58c995486fc93a242b987640b692db8c</sid><ORCID>0000-0003-2157-9157</ORCID><firstname>Owain</firstname><surname>Howell</surname><name>Owain Howell</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2023-09-12</date><deptcode>BMS</deptcode><abstract>Microglial activation plays central roles in neuroinflammatory and neurodegenerative diseases. Positron emission tomography (PET) targeting 18 kDa Translocator Protein (TSPO) is widely used for localising inflammation in vivo, but its quantitative interpretation remains uncertain. We show that TSPO expression increases in activated microglia in mouse brain disease models but does not change in a non-human primate disease model or in common neurodegenerative and neuroinflammatory human diseases. We describe genetic divergence in the TSPO gene promoter, consistent with the hypothesis that the increase in TSPO expression in activated myeloid cells depends on the transcription factor AP1 and is unique to a subset of rodent species within the Muroidea superfamily. Finally, we identify LCP2 and TFEC as potential markers of microglial activation in humans. These data emphasise that TSPO expression in human myeloid cells is related to different phenomena than in mice, and that TSPO-PET signals in humans reflect the density of inflammatory cells rather than activation state.</abstract><type>Journal Article</type><journal>Nature Communications</journal><volume>14</volume><journalNumber>1</journalNumber><paginationStart/><paginationEnd/><publisher>Springer Science and Business Media LLC</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2041-1723</issnElectronic><keywords>Translocator protein, TSPO, positron emission tomography, PET, neurodegenerative diseases, neuroinflammatory diseases, microglial activation</keywords><publishedDay>28</publishedDay><publishedMonth>8</publishedMonth><publishedYear>2023</publishedYear><publishedDate>2023-08-28</publishedDate><doi>10.1038/s41467-023-40937-z</doi><url>http://dx.doi.org/10.1038/s41467-023-40937-z</url><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm/><funders>The authors thank the UK MS Society for financial support (grant number: C008-16.1). DRO was funded by an MRC Clinician Scientist Award (MR/N008219/1). P.M.M. acknowledges generous support from Edmond J Safra Foundation and Lily Safra, the NIHR Senior Investigator programme and the UK Dementia Research Institute which receives its funding from DRI Ltd., funded by the UK Medical Research Council, Alzheimer’s Society, and Alzheimer’s Research UK. P.M.M. and D.R.O. thank the Imperial College Healthcare Trust-NIHR Biomedical Research Centre for infrastructure support and the Medical Research Council for support of TSPO studies (MR/N016343/1). E.A. was supported by the ALS Stichting (grant “The Dutch ALS Tissue Bank”). Dr. Sally Cowley (Oxford Parkinson’s Disease Centre, James Martin Stem Cell Facility, University of Oxford) provided the iPS cell line and expertise in differentiation to iPS-microglia. All authors thank the NIHR Imperial Clinical Research Facility (ICRF) for supporting procedures relating to collection of blood samples. P.M. and B.B.T. are funded by the Swiss National Science Foundation (projects 320030_184713 and 310030_212322, respectively). S.T. was supported by an “Early Postdoc.Mobility” scholarship (P2GEP3_191446) from the Swiss National Science Foundation, a “Clinical Medicine Plus” scholarship from the Prof Dr. Max Cloëtta Foundation (Zurich, Switzerland), from the Jean et Madeleine Vachoux Foundation (Geneva, Switzerland) and from the University Hospitals of Geneva. The authors wish to thank Pia Lovero and Adrien Fischer for expert technical assistance. The results published here are in part based on data obtained from the AD Knowledge Portal (https://adknowledgeportal.org). Study data were generated from postmortem brain tissue provided by the Religious Orders Study and Rush Memory and Aging Project (ROSMAP) cohort at Rush Alzheimer’s Disease Center, Rush University Medical Center, Chicago. This work was funded by NIH grants U01AG061356 (De Jager/Bennett), RF1AG057473 (De Jager/Bennett), and U01AG046152 (De Jager/Bennett) as part of the AMP-AD consortium, as well as NIH grants R01AG066831 (Menon) and U01AG072572 (De Jager/St George-Hyslop).</funders><projectreference/><lastEdited>2024-02-01T16:05:12.8644746</lastEdited><Created>2023-09-12T09:33:22.8297880</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Biomedical Science</level></path><authors><author><firstname>Erik</firstname><surname>Nutma</surname><orcid>0000-0002-7332-1636</orcid><order>1</order></author><author><firstname>Nurun</firstname><surname>Fancy</surname><orcid>0000-0002-6481-6266</orcid><order>2</order></author><author><firstname>Maria</firstname><surname>Weinert</surname><orcid>0000-0001-6187-1000</orcid><order>3</order></author><author><firstname>Stergios</firstname><surname>Tsartsalis</surname><orcid>0000-0002-6565-6313</orcid><order>4</order></author><author><firstname>Manuel C.</firstname><surname>Marzin</surname><order>5</order></author><author><firstname>Robert C. J.</firstname><surname>Muirhead</surname><order>6</order></author><author><firstname>Irene</firstname><surname>Falk</surname><order>7</order></author><author><firstname>Marjolein</firstname><surname>Breur</surname><order>8</order></author><author><firstname>Joy de</firstname><surname>Bruin</surname><order>9</order></author><author><firstname>David</firstname><surname>Hollaus</surname><order>10</order></author><author><firstname>Robin</firstname><surname>Pieterman</surname><order>11</order></author><author><firstname>Jasper</firstname><surname>Anink</surname><order>12</order></author><author><firstname>David</firstname><surname>Story</surname><order>13</order></author><author><firstname>Siddharthan</firstname><surname>Chandran</surname><order>14</order></author><author><firstname>Jiabin</firstname><surname>Tang</surname><order>15</order></author><author><firstname>Maria 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A.</firstname><surname>Galloway</surname><order>25</order></author><author><firstname>Rochelle Y.</firstname><surname>Benoit</surname><order>26</order></author><author><firstname>Quentin</firstname><surname>Amossé</surname><orcid>0000-0002-5553-9594</orcid><order>27</order></author><author><firstname>Kelly</firstname><surname>Ceyzériat</surname><order>28</order></author><author><firstname>Aurélien M.</firstname><surname>Badina</surname><orcid>0009-0005-1890-8986</orcid><order>29</order></author><author><firstname>Enikö</firstname><surname>Kövari</surname><order>30</order></author><author><firstname>Caterina</firstname><surname>Bendotti</surname><orcid>0000-0003-1055-1271</orcid><order>31</order></author><author><firstname>Eleonora</firstname><surname>Aronica</surname><orcid>0000-0002-3542-3770</orcid><order>32</order></author><author><firstname>Carola I.</firstname><surname>Radulescu</surname><order>33</order></author><author><firstname>Jia 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v2 64510 2023-09-12 Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases 58c995486fc93a242b987640b692db8c 0000-0003-2157-9157 Owain Howell Owain Howell true false 2023-09-12 BMS Microglial activation plays central roles in neuroinflammatory and neurodegenerative diseases. Positron emission tomography (PET) targeting 18 kDa Translocator Protein (TSPO) is widely used for localising inflammation in vivo, but its quantitative interpretation remains uncertain. We show that TSPO expression increases in activated microglia in mouse brain disease models but does not change in a non-human primate disease model or in common neurodegenerative and neuroinflammatory human diseases. We describe genetic divergence in the TSPO gene promoter, consistent with the hypothesis that the increase in TSPO expression in activated myeloid cells depends on the transcription factor AP1 and is unique to a subset of rodent species within the Muroidea superfamily. Finally, we identify LCP2 and TFEC as potential markers of microglial activation in humans. These data emphasise that TSPO expression in human myeloid cells is related to different phenomena than in mice, and that TSPO-PET signals in humans reflect the density of inflammatory cells rather than activation state. Journal Article Nature Communications 14 1 Springer Science and Business Media LLC 2041-1723 Translocator protein, TSPO, positron emission tomography, PET, neurodegenerative diseases, neuroinflammatory diseases, microglial activation 28 8 2023 2023-08-28 10.1038/s41467-023-40937-z http://dx.doi.org/10.1038/s41467-023-40937-z COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University The authors thank the UK MS Society for financial support (grant number: C008-16.1). DRO was funded by an MRC Clinician Scientist Award (MR/N008219/1). P.M.M. acknowledges generous support from Edmond J Safra Foundation and Lily Safra, the NIHR Senior Investigator programme and the UK Dementia Research Institute which receives its funding from DRI Ltd., funded by the UK Medical Research Council, Alzheimer’s Society, and Alzheimer’s Research UK. P.M.M. and D.R.O. thank the Imperial College Healthcare Trust-NIHR Biomedical Research Centre for infrastructure support and the Medical Research Council for support of TSPO studies (MR/N016343/1). E.A. was supported by the ALS Stichting (grant “The Dutch ALS Tissue Bank”). Dr. Sally Cowley (Oxford Parkinson’s Disease Centre, James Martin Stem Cell Facility, University of Oxford) provided the iPS cell line and expertise in differentiation to iPS-microglia. All authors thank the NIHR Imperial Clinical Research Facility (ICRF) for supporting procedures relating to collection of blood samples. P.M. and B.B.T. are funded by the Swiss National Science Foundation (projects 320030_184713 and 310030_212322, respectively). S.T. was supported by an “Early Postdoc.Mobility” scholarship (P2GEP3_191446) from the Swiss National Science Foundation, a “Clinical Medicine Plus” scholarship from the Prof Dr. Max Cloëtta Foundation (Zurich, Switzerland), from the Jean et Madeleine Vachoux Foundation (Geneva, Switzerland) and from the University Hospitals of Geneva. The authors wish to thank Pia Lovero and Adrien Fischer for expert technical assistance. The results published here are in part based on data obtained from the AD Knowledge Portal (https://adknowledgeportal.org). Study data were generated from postmortem brain tissue provided by the Religious Orders Study and Rush Memory and Aging Project (ROSMAP) cohort at Rush Alzheimer’s Disease Center, Rush University Medical Center, Chicago. This work was funded by NIH grants U01AG061356 (De Jager/Bennett), RF1AG057473 (De Jager/Bennett), and U01AG046152 (De Jager/Bennett) as part of the AMP-AD consortium, as well as NIH grants R01AG066831 (Menon) and U01AG072572 (De Jager/St George-Hyslop). 2024-02-01T16:05:12.8644746 2023-09-12T09:33:22.8297880 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Erik Nutma 0000-0002-7332-1636 1 Nurun Fancy 0000-0002-6481-6266 2 Maria Weinert 0000-0001-6187-1000 3 Stergios Tsartsalis 0000-0002-6565-6313 4 Manuel C. Marzin 5 Robert C. J. Muirhead 6 Irene Falk 7 Marjolein Breur 8 Joy de Bruin 9 David Hollaus 10 Robin Pieterman 11 Jasper Anink 12 David Story 13 Siddharthan Chandran 14 Jiabin Tang 15 Maria C. Trolese 0000-0003-4471-2491 16 Takashi Saito 0000-0002-9659-9251 17 Takaomi C. Saido 18 Katharine H. Wiltshire 19 Paula Beltran-Lobo 20 Alexandra Phillips 21 Jack Antel 0000-0002-5148-0636 22 Luke Healy 0000-0001-9496-2216 23 Marie-France Dorion 24 Dylan A. Galloway 25 Rochelle Y. Benoit 26 Quentin Amossé 0000-0002-5553-9594 27 Kelly Ceyzériat 28 Aurélien M. Badina 0009-0005-1890-8986 29 Enikö Kövari 30 Caterina Bendotti 0000-0003-1055-1271 31 Eleonora Aronica 0000-0002-3542-3770 32 Carola I. Radulescu 33 Jia Hui Wong 0000-0002-7036-8121 34 Anna M. Barron 0000-0002-4715-9364 35 Amy M. Smith 36 Samuel J. Barnes 0000-0003-4030-6453 37 David W. Hampton 38 Paul van der Valk 39 Steven Jacobson 40 Owain Howell 0000-0003-2157-9157 41 David Baker 42 Markus Kipp 0000-0001-5043-9052 43 Hannes Kaddatz 0000-0003-1927-7344 44 Benjamin B. Tournier 0000-0002-8027-7530 45 Philippe Millet 0000-0002-5803-0478 46 Paul M. Matthews 0000-0002-1619-8328 47 Craig S. Moore 0000-0003-3333-435x 48 Sandra Amor 49 David R. Owen 0000-0002-1198-7563 50 64510__28701__5fe55ad798f743b487bef368d4ae4064.pdf 64510.VOR.pdf 2023-10-04T14:07:01.6853171 Output 9031134 application/pdf Version of Record true © The Author(s) 2023. Distributed under the terms of a Creative Commons Attribution 4.0 License (CC BY 4.0). true eng https://creativecommons.org/licenses/by/4.0/ |
| title |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
| spellingShingle |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases Owain Howell |
| title_short |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
| title_full |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
| title_fullStr |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
| title_full_unstemmed |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
| title_sort |
Translocator protein is a marker of activated microglia in rodent models but not human neurodegenerative diseases |
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58c995486fc93a242b987640b692db8c |
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58c995486fc93a242b987640b692db8c_***_Owain Howell |
| author |
Owain Howell |
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Erik Nutma Nurun Fancy Maria Weinert Stergios Tsartsalis Manuel C. Marzin Robert C. J. Muirhead Irene Falk Marjolein Breur Joy de Bruin David Hollaus Robin Pieterman Jasper Anink David Story Siddharthan Chandran Jiabin Tang Maria C. Trolese Takashi Saito Takaomi C. Saido Katharine H. Wiltshire Paula Beltran-Lobo Alexandra Phillips Jack Antel Luke Healy Marie-France Dorion Dylan A. Galloway Rochelle Y. Benoit Quentin Amossé Kelly Ceyzériat Aurélien M. Badina Enikö Kövari Caterina Bendotti Eleonora Aronica Carola I. Radulescu Jia Hui Wong Anna M. Barron Amy M. Smith Samuel J. Barnes David W. Hampton Paul van der Valk Steven Jacobson Owain Howell David Baker Markus Kipp Hannes Kaddatz Benjamin B. Tournier Philippe Millet Paul M. Matthews Craig S. Moore Sandra Amor David R. Owen |
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2023 |
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10.1038/s41467-023-40937-z |
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Microglial activation plays central roles in neuroinflammatory and neurodegenerative diseases. Positron emission tomography (PET) targeting 18 kDa Translocator Protein (TSPO) is widely used for localising inflammation in vivo, but its quantitative interpretation remains uncertain. We show that TSPO expression increases in activated microglia in mouse brain disease models but does not change in a non-human primate disease model or in common neurodegenerative and neuroinflammatory human diseases. We describe genetic divergence in the TSPO gene promoter, consistent with the hypothesis that the increase in TSPO expression in activated myeloid cells depends on the transcription factor AP1 and is unique to a subset of rodent species within the Muroidea superfamily. Finally, we identify LCP2 and TFEC as potential markers of microglial activation in humans. These data emphasise that TSPO expression in human myeloid cells is related to different phenomena than in mice, and that TSPO-PET signals in humans reflect the density of inflammatory cells rather than activation state. |
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2023-08-28T16:05:13Z |
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