Citation: Riolo, G.; Ricci, C.; De
Angelis, N.; Marzocchi, C.; Guerrera,
G.; Borsellino, G.; Giannini, F.;
Battistini, S. BDNF and Pro-BDNF in
Amyotrophic Lateral Sclerosis: A
New Perspective for Biomarkers of
Neurodegeneration. Brain Sci. 2022,
12, 617. https://doi.org/10.3390/
brainsci12050617
Academic Editor: Chiara Villa
Received: 30 March 2022
Accepted: 6 May 2022
Published: 9 May 2022
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brain
sciences
Article
BDNF and Pro-BDNF in Amyotrophic Lateral Sclerosis: A New
Perspective for Biomarkers of Neurodegeneration
Giulia Riolo
1
, Claudia Ricci
1,
* , Nicoletta De Angelis
1
, Carlotta Marzocchi
1
, Gisella Guerrera
2
,
Giovanna Borsellino
2
, Fabio Giannini
1
and Stefania Battistini
1
1
Department of Medical, Surgical and Neurological Sciences, University of Siena, 53100 Siena, Italy;
giulia.riolo@gmail.com (G.R.); nicoletta.deangelis91@gmail.com (N.D.A.); carlottamarzocchi@libero.it (C.M.);
fabio.giannini@unisi.it (F.G.); stefania.battistini@unisi.it (S.B.)
2
Neuroimmunology Unit, Santa Lucia Foundation IRCCS, 00143 Rome, Italy; g.guerrera@hsantalucia.it (G.G.);
g.borsellino@hsantalucia.it (G.B.)
* Correspondence: claudia.ricci@unisi.it
Abstract: Amyotrophic Lateral Sclerosis (ALS) is characterized by the progressive degeneration of
upper or lower motor neurons, leading to muscle wasting and paralysis, resulting in respiratory
failure and death. The precise ALS aetiology is poorly understood, mainly due to clinical and genetic
heterogeneity. Thus, the identification of reliable biomarkers of disease could be helpful in clinical
practice. In this study, we investigated whether the levels of brain-derived neurotrophic factor (BDNF)
and its precursor Pro-BDNF in serum and cerebrospinal fluid (CSF) may reflect the pathological
changes related to ALS. We found higher BDNF and lower Pro-BDNF levels in ALS sera compared to
healthy controls. BDNF/Pro-BDNF ratio turned out to be accurate in distinguishing ALS patients
from controls. Then, the correlations of these markers with several ALS clinical variables were
evaluated. This analysis revealed three statistically significant associations: (1) Patients carrying the
C9orf72 expansion significantly differed from non-carrier patients and showed serum BDNF levels
comparable to control subjects; (2) BDNF levels in CSF were significantly higher in ALS patients
with faster disease progression; (3) lower serum levels of Pro-BDNF were associated with a shorter
survival. Therefore, we suggest that BDNF and Pro-BDNF, alone or in combination, might be used as
ALS prognostic biomarkers.
Keywords: Amyotrophic Lateral Sclerosis; BDNF; Pro-BDNF; biomarkers; disease progression;
CSF; serum
1. Introduction
Amyotrophic Lateral Sclerosis (ALS) is a heterogeneous condition resulting from the
progressive degeneration of motor neurons in the brain and spinal cord. The classical
disease has a focal onset, characterized by the loss of function of upper or lower motor
neurons, resulting in no muscle nourishment and leading to inevitable paralysis [1,2].
Importantly, atrophy quickly progresses from the region of onset to close spinal regions
and very often the failure of respiratory muscles is fatal for ALS patients [3]. Riluzole and
edaravone, the only FDA approved drugs so far, marginally enhance survival and slow
the clinical progression of the disease, increasing the urgency for new effective therapeutic
treatments [4].
The worldwide incidence of ALS accounts for 1.6/100,000 people each year [5]. Al-
most 90% of cases are classified as sporadic (sALS) and only the remaining 10% have a
family history of disease (fALS), characterized by a Mendelian dominant inheritance with
incomplete penetrance [6].
Despite decades of research, the precise aetiology of ALS is definitely poorly under-
stood. Diagnosis, commonly made with a considerable delay from symptom onset, is
mostly based on electrophysiological examinations and clinical judgment, because there is
Brain Sci. 2022, 12, 617. https://doi.org/10.3390/brainsci12050617 https://www.mdpi.com/journal/brainsci