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A systematic review of progranulin concentrations in biofluids in over 7,000 people-assessing the pathogenicity of GRN mutations and other influencing factors
IJ. Swift, R. Rademakers, N. Finch, M. Baker, R. Ghidoni, L. Benussi, G. Binetti, G. Rossi, M. Synofzik, C. Wilke, D. Mengel, C. Graff, LT. Takada, R. Sánchez-Valle, A. Antonell, D. Galimberti, C. Fenoglio, M. Serpente, M. Arcaro, S. Schreiber,...
Language English Country England, Great Britain
Document type Systematic Review, Journal Article
Grant support
2019-02248
JPND GENFI-PROX grant
2019-02248
JPND GENFI-PROX grant
2019-02248
JPND GENFI-PROX grant
2019-02248
JPND GENFI-PROX grant
2019-02248
JPND GENFI-PROX grant
2019-02248
JPND GENFI-PROX grant
MR/M008525/1
MRC Clinician Scientist Fellowship
MR/M008525/1
MRC Clinician Scientist Fellowship
2013/017584
FAPESP grant number
01ED2008A
EU Joint Programme-Neurodegenerative Diseases networks Genfi-Prox
01ED2001
bPride
FTLDc 01GI1007A, Moodmarker 01EW200
German Federal Ministry of Education and Research
MIRIADE 860197, FAIR-PARK II 633190
the EU
SFB1279
German Research Foundation/DFG
D.3830
The foundation of the state Baden-Württemberg
D.5009
Boehringer Ingelheim Ulm University BioCenter and the Thierry Latran Foundation
#ALFGBG-71320
Swedish State Support for Clinical Research
#201809-2016862
Alzheimer Drug Discovery Foundation (ADDF), USA
#ADSF-21-831376-C, #ADSF-21-831381-C, #ADSF-21-831377-C
AD Strategic Fund and the Alzheimer's Association
#2019-02397, #2022-01018
Swedish Research Council
#FO2022-0270
the Bluefield Project, the Olav Thon Foundation, the Erling-Persson Family Foundation, Stiftelsen för Gamla Tjänarinnor, Hjärnfonden, Sweden
JPND2021-00694)
the European Union Joint Programme - Neurodegenerative Disease Research
UKDRI-1003
UK Dementia Research Institute at UCL
ARUK-RADF2021A-003
Alzheimer's Research UK
BRC149/NS/MH
NIHR Rare Disease Translational Research Collaboration
MR/M023664/1
MRC UK GENFI grant
NLK
BioMedCentral
from 2009-06-01
BioMedCentral Open Access
from 2009
Directory of Open Access Journals
from 2009
Free Medical Journals
from 2009
PubMed Central
from 2009
ProQuest Central
from 2015-01-01
Open Access Digital Library
from 2009-01-01
Open Access Digital Library
from 2009-01-01
Health & Medicine (ProQuest)
from 2015-01-01
ROAD: Directory of Open Access Scholarly Resources
from 2009
Springer Nature OA/Free Journals
from 2009-06-01
- MeSH
- Frontotemporal Dementia * genetics pathology MeSH
- Humans MeSH
- Membrane Proteins genetics MeSH
- Intercellular Signaling Peptides and Proteins genetics MeSH
- Mutation genetics MeSH
- Progranulins genetics MeSH
- Nerve Tissue Proteins genetics MeSH
- Virulence MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Systematic Review MeSH
BACKGROUND: Pathogenic heterozygous mutations in the progranulin gene (GRN) are a key cause of frontotemporal dementia (FTD), leading to significantly reduced biofluid concentrations of the progranulin protein (PGRN). This has led to a number of ongoing therapeutic trials aiming to treat this form of FTD by increasing PGRN levels in mutation carriers. However, we currently lack a complete understanding of factors that affect PGRN levels and potential variation in measurement methods. Here, we aimed to address this gap in knowledge by systematically reviewing published literature on biofluid PGRN concentrations. METHODS: Published data including biofluid PGRN concentration, age, sex, diagnosis and GRN mutation were collected for 7071 individuals from 75 publications. The majority of analyses (72%) had focused on plasma PGRN concentrations, with many of these (56%) measured with a single assay type (Adipogen) and so the influence of mutation type, age at onset, sex, and diagnosis were investigated in this subset of the data. RESULTS: We established a plasma PGRN concentration cut-off between pathogenic mutation carriers and non-carriers of 74.8 ng/mL using the Adipogen assay based on 3301 individuals, with a CSF concentration cut-off of 3.43 ng/mL. Plasma PGRN concentration varied by GRN mutation type as well as by clinical diagnosis in those without a GRN mutation. Plasma PGRN concentration was significantly higher in women than men in GRN mutation carriers (p = 0.007) with a trend in non-carriers (p = 0.062), and there was a significant but weak positive correlation with age in both GRN mutation carriers and non-carriers. No significant association was seen with weight or with TMEM106B rs1990622 genotype. However, higher plasma PGRN levels were seen in those with the GRN rs5848 CC genotype in both GRN mutation carriers and non-carriers. CONCLUSIONS: These results further support the usefulness of PGRN concentration for the identification of the large majority of pathogenic mutations in the GRN gene. Furthermore, these results highlight the importance of considering additional factors, such as mutation type, sex and age when interpreting PGRN concentrations. This will be particularly important as we enter the era of trials for progranulin-associated FTD.
A and G Pharmaceutical Inc Columbia MD USA
Autonomous University of Barcelona 08913 Barcelona Spain
Center of Pediatric Research University of Leipzig Leipzig Germany
Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas 28031 Madrid Spain
Centro de Investigación Biomédica en Red Sobre Enfermedades Neurodegenerativas Madrid Spain
Clinical Neurochemistry Laboratory Sahlgrenska University Hospital Mölndal Sweden
Department of Biomedical Sciences University of Antwerp Antwerp Belgium
Department of Clinical and Experimental Sciences University of Brescia Brescia Italy
Department of Neonatology Tuebingen University Hospital Tuebingen Germany
Department of Nephrology Faculty of Medicine Juntendo University Tokyo Japan
Department of Neurological and Vision Sciences Neurophysiology Unit ASST SpedaliCivili Brescia Italy
Department of Neurology and Clinical Neurophysiology Trondheim University Hospital Trondheim Norway
Department of Neurology Fundación Jiménez Díaz Madrid Spain
Department of Neurology Klinikum Rechts Der Isar Technical University of Munich Munich Germany
Department of Neurology Mayo Clinic Jacksonville FL USA
Department of Neurology Mayo Clinic Rochester MN USA
Department of Neurology Otto Von Guericke University Magdeburg Germany
Department of Neurology University of California Los Angeles California USA
Department of Neurology University of Colorado Anschutz Medical Campus Denver CO USA
Department of Neuroscience Mayo Clinic Jacksonville FL USA
Department of Obstetrics and Gynecology Rostock University Medical Center Rostock Germany
Department of Oncology Mayo Clinic Rochester MN USA
Department of Orthopaedics and Rehabilitation Yale University School of Medicine New Haven CT USA
Department of Psychiatry Hospital in Tauberbischofsheim Tauberbischofsheim Germany
Department of Psychiatry University College Cork Cork Ireland
Department of Research Trondheim University Hospital Trondheim Norway
Department of Urology Martin Luther University Halle Wittenberg Halle Germany
Dept of Biomedical Surgical and Dental Sciences University of Milan Milan Italy
DZNE German Center for Neurodegenerative Diseases Tübingen Germany
Faculty of Medicine University of Coimbra Coimbra Portugal
German Center of Neurodegenerative Diseases Tübingen Germany
Hong Kong Center for Neurodegenerative Diseases Hong Kong China
Hospital for Children and Adolescents University of Leipzig Leipzig Germany
Institute of Rheumatology Na Slupi 4 12850 Prague 2 Prague Czech Republic
Leipzig Research Center for Civilization Diseases LIFE University of Leipzig Leipzig Germany
Neurology Department Centro Hospitalar E Universitário de Coimbra Coimbra Portugal
Neurology Department Hospital Sant Pau Memory Unit Barcelona Spain
Neuroscience Area Biodonostia Health Research Insitute San Sebastian Gipuzkoa Spain
Program in Oncology University of Maryland Greenebaum Comprehensive Cancer Center Baltimore MD USA
Regional Neurogenetic Centre ASPCZ Lamezia Terme Italy
Unit of Neurology 5 and Neuropathology Fondazione IRCCS Istituto Neurologico Carlo Besta Milan Italy
University of Pennsylvania Gene Therapy Program Philadelphia USA
References provided by Crossref.org
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- $a A systematic review of progranulin concentrations in biofluids in over 7,000 people-assessing the pathogenicity of GRN mutations and other influencing factors / $c IJ. Swift, R. Rademakers, N. Finch, M. Baker, R. Ghidoni, L. Benussi, G. Binetti, G. Rossi, M. Synofzik, C. Wilke, D. Mengel, C. Graff, LT. Takada, R. Sánchez-Valle, A. Antonell, D. Galimberti, C. Fenoglio, M. Serpente, M. Arcaro, S. Schreiber, S. Vielhaber, P. Arndt, I. Santana, MR. Almeida, F. Moreno, M. Barandiaran, A. Gabilondo, J. Stubert, E. Gómez-Tortosa, P. Agüero, MJ. Sainz, T. Gohda, M. Murakoshi, N. Kamei, S. Kittel-Schneider, A. Reif, J. Weigl, J. Jian, C. Liu, G. Serrero, T. Greither, G. Theil, E. Lohmann, S. Gazzina, S. Bagnoli, G. Coppola, A. Bruni, M. Quante, W. Kiess, A. Hiemisch, A. Jurkutat, MS. Block, AM. Carlson, G. Bråthen, SB. Sando, GR. Grøntvedt, C. Lauridsen, A. Heslegrave, C. Heller, E. Abel, A. Gómez-Núñez, R. Puey, A. Arighi, E. Rotondo, LC. Jiskoot, LHH. Meeter, J. Durães, M. Lima, M. Tábuas-Pereira, J. Lemos, B. Boeve, RC. Petersen, DW. Dickson, NR. Graff-Radford, I. LeBer, L. Sellami, F. Lamari, F. Clot, B. Borroni, V. Cantoni, J. Rivolta, A. Lleó, J. Fortea, D. Alcolea, I. Illán-Gala, L. Andres-Cerezo, P. Van Damme, J. Clarimon, P. Steinacker, E. Feneberg, M. Otto, EL. van der Ende, JC. van Swieten, H. Seelaar, H. Zetterberg, A. Sogorb-Esteve, JD. Rohrer
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- $a BACKGROUND: Pathogenic heterozygous mutations in the progranulin gene (GRN) are a key cause of frontotemporal dementia (FTD), leading to significantly reduced biofluid concentrations of the progranulin protein (PGRN). This has led to a number of ongoing therapeutic trials aiming to treat this form of FTD by increasing PGRN levels in mutation carriers. However, we currently lack a complete understanding of factors that affect PGRN levels and potential variation in measurement methods. Here, we aimed to address this gap in knowledge by systematically reviewing published literature on biofluid PGRN concentrations. METHODS: Published data including biofluid PGRN concentration, age, sex, diagnosis and GRN mutation were collected for 7071 individuals from 75 publications. The majority of analyses (72%) had focused on plasma PGRN concentrations, with many of these (56%) measured with a single assay type (Adipogen) and so the influence of mutation type, age at onset, sex, and diagnosis were investigated in this subset of the data. RESULTS: We established a plasma PGRN concentration cut-off between pathogenic mutation carriers and non-carriers of 74.8 ng/mL using the Adipogen assay based on 3301 individuals, with a CSF concentration cut-off of 3.43 ng/mL. Plasma PGRN concentration varied by GRN mutation type as well as by clinical diagnosis in those without a GRN mutation. Plasma PGRN concentration was significantly higher in women than men in GRN mutation carriers (p = 0.007) with a trend in non-carriers (p = 0.062), and there was a significant but weak positive correlation with age in both GRN mutation carriers and non-carriers. No significant association was seen with weight or with TMEM106B rs1990622 genotype. However, higher plasma PGRN levels were seen in those with the GRN rs5848 CC genotype in both GRN mutation carriers and non-carriers. CONCLUSIONS: These results further support the usefulness of PGRN concentration for the identification of the large majority of pathogenic mutations in the GRN gene. Furthermore, these results highlight the importance of considering additional factors, such as mutation type, sex and age when interpreting PGRN concentrations. This will be particularly important as we enter the era of trials for progranulin-associated FTD.
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