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@ARTICLE{Schls:139656,
author = {Schöls, Ludger and Rattay, Tim W and Martus, Peter and
Meisner, Christoph and Baets, Jonathan and Fischer, Imma and
Jägle, Christine and Fraidakis, Matthew J and Martinuzzi,
Andrea and Saute, Jonas Alex and Scarlato, Marina and
Antenora, Antonella and Stendel, Claudia and Höflinger,
Philip and Lourenco, Charles Marques and Abreu, Lisa and
Smets, Katrien and Paucar, Martin and Deconinck, Tine and
Bis, Dana M and Wiethoff, Sarah and Bauer, Peter and
Arnoldi, Alessia and Marques, Wilson and Jardim, Laura
Bannach and Hauser, Stefan and Criscuolo, Chiara and Filla,
Alessandro and Züchner, Stephan and Bassi, Maria Teresa and
Klopstock, Thomas and De Jonghe, Peter and Björkhem,
Ingemar and Schüle, Rebecca},
title = {{H}ereditary spastic paraplegia type 5: natural history,
biomarkers and a randomized controlled trial.},
journal = {Brain},
volume = {140},
number = {12},
issn = {0006-8950},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {DZNE-2020-05978},
pages = {3112-3127},
year = {2017},
abstract = {Spastic paraplegia type 5 (SPG5) is a rare subtype of
hereditary spastic paraplegia, a highly heterogeneous group
of neurodegenerative disorders defined by progressive
neurodegeneration of the corticospinal tract motor neurons.
SPG5 is caused by recessive mutations in the gene CYP7B1
encoding oxysterol-7α-hydroxylase. This enzyme is involved
in the degradation of cholesterol into primary bile acids.
CYP7B1 deficiency has been shown to lead to accumulation of
neurotoxic oxysterols. In this multicentre study, we have
performed detailed clinical and biochemical analysis in 34
genetically confirmed SPG5 cases from 28 families, studied
dose-dependent neurotoxicity of oxysterols in human cortical
neurons and performed a randomized placebo-controlled double
blind interventional trial targeting oxysterol accumulation
in serum of SPG5 patients. Clinically, SPG5 manifested in
childhood or adolescence (median 13 years). Gait ataxia was
a common feature. SPG5 patients lost the ability to walk
independently after a median disease duration of 23 years
and became wheelchair dependent after a median 33 years. The
overall cross-sectional progression rate of 0.56 points on
the Spastic Paraplegia Rating Scale per year was slightly
lower than the longitudinal progression rate of 0.80 points
per year. Biochemically, marked accumulation of CYP7B1
substrates including 27-hydroxycholesterol was confirmed in
serum (n = 19) and cerebrospinal fluid (n = 17) of SPG5
patients. Moreover, 27-hydroxycholesterol levels in serum
correlated with disease severity and disease duration.
Oxysterols were found to impair metabolic activity and
viability of human cortical neurons at concentrations found
in SPG5 patients, indicating that elevated levels of
oxysterols might be key pathogenic factors in SPG5. We thus
performed a randomized placebo-controlled trial (EudraCT
2015-000978-35) with atorvastatin 40 mg/day for 9 weeks in
14 SPG5 patients with 27-hydroxycholesterol levels in serum
as the primary outcome measure. Atorvastatin, but not
placebo, reduced serum 27-hydroxycholesterol from 853 ng/ml
[interquartile range (IQR) 683-1113] to 641 (IQR 507-694)
$(-31.5\%,$ P = 0.001, Mann-Whitney U-test). Similarly,
25-hydroxycholesterol levels in serum were reduced. In
cerebrospinal fluid 27-hydroxycholesterol was reduced by
$8.4\%$ but this did not significantly differ from placebo.
As expected, no effects were seen on clinical outcome
parameters in this short-term trial. In this study, we
define the mutational and phenotypic spectrum of SPG5,
examine the correlation of disease severity and progression
with oxysterol concentrations, and demonstrate in a
randomized controlled trial that atorvastatin treatment can
effectively lower 27-hydroxycholesterol levels in serum of
SPG5 patients. We thus demonstrate the first causal
treatment strategy in hereditary spastic paraplegia.},
keywords = {Adolescent / Adult / Atorvastatin: therapeutic use /
Biomarkers: blood / Biomarkers: cerebrospinal fluid /
Case-Control Studies / Cell Proliferation / Cross-Sectional
Studies / Cytochrome P450 Family 7: genetics / Disease
Progression / Double-Blind Method / Family / Female / Humans
/ Hydroxycholesterols: metabolism /
Hydroxymethylglutaryl-CoA Reductase Inhibitors: therapeutic
use / Induced Pluripotent Stem Cells / Male / Middle Aged /
Mutation / Neurites / Oxysterols: blood / Oxysterols:
cerebrospinal fluid / Pedigree / Severity of Illness Index /
Spastic Paraplegia, Hereditary: drug therapy / Spastic
Paraplegia, Hereditary: genetics / Spastic Paraplegia,
Hereditary: metabolism / Steroid Hydroxylases: genetics /
Young Adult / Biomarkers (NLM Chemicals) /
Hydroxycholesterols (NLM Chemicals) /
Hydroxymethylglutaryl-CoA Reductase Inhibitors (NLM
Chemicals) / Oxysterols (NLM Chemicals) /
27-hydroxycholesterol (NLM Chemicals) /
25-hydroxycholesterol (NLM Chemicals) / Atorvastatin (NLM
Chemicals) / Steroid Hydroxylases (NLM Chemicals) /
Cytochrome P450 Family 7 (NLM Chemicals) / CYP7B1 protein,
human (NLM Chemicals)},
cin = {AG Schöls / AG Gasser / AG Höglinger 1 / AG Levin},
ddc = {610},
cid = {I:(DE-2719)5000005 / I:(DE-2719)1210000 /
I:(DE-2719)1110002 / I:(DE-2719)1111016},
pnm = {344 - Clinical and Health Care Research (POF3-344) / 345 -
Population Studies and Genetics (POF3-345)},
pid = {G:(DE-HGF)POF3-344 / G:(DE-HGF)POF3-345},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:29126212},
pmc = {pmc:PMC5841036},
doi = {10.1093/brain/awx273},
url = {https://pub.dzne.de/record/139656},
}