Citation: Bufalo, M.C.; Almeida,
M.E.S.d.; Jensen, J.R.;
DeOcesano-Pereira, C.; Lichtenstein,
F.; Picolo, G.; Chudzinski-Tavassi,
A.M.; Sampaio, S.C.; Cury, Y.;
Zambelli, V.O. Human Sensory
Neuron-like Cells and Glycated
Collagen Matrix as a Model for the
Screening of Analgesic Compounds.
Cells 2022, 11, 247. https://doi.org/
10.3390/cells11020247
Academic Editor: Albert Quintana
Received: 15 December 2021
Accepted: 8 January 2022
Published: 12 January 2022
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cells
Article
Human Sensory Neuron-like Cells and Glycated Collagen
Matrix as a Model for the Screening of Analgesic Compounds
Michelle Cristiane Bufalo
1,2
, Maíra Estanislau Soares de Almeida
2,3
, José Ricardo Jensen
4
,
Carlos DeOcesano-Pereira
2
, Flavio Lichtenstein
2
, Gisele Picolo
1
, Ana Marisa Chudzinski-Tavassi
2,5
,
Sandra Coccuzzo Sampaio
3,6
, Yara Cury
1,
* and Vanessa Olzon Zambelli
1,2,
*
1
Laboratory of Pain and Signaling, Butantan Institute, São Paulo 05503-900, Brazil;
michelle.bufalo@butantan.gov.br (M.C.B.); gisele.picolo@butantan.gov.br (G.P.)
2
Center of Excellence in New Target Discovery, Butantan Institute, São Paulo 05503-900, Brazil;
mesalmeida@gmail.com (M.E.S.d.A.); carlos.ocesano@butantan.gov.br (C.D.-P.);
flavio.lichtenstein@butantan.gov.br (F.L.); ana.chudzinski@butantan.gov.br (A.M.C.-T.)
3
Laboratory of Pathophysiology, Butantan Institute, São Paulo 05503-900, Brazil;
sandra.coccuzzo@butantan.gov.br
4
Immunogenetics Laboratory, Butantan Institute, São Paulo 05503-900, Brazil; jose.jensen@butantan.gov.br
5
Innovation and Development Laboratory, Innovation and Development Center, Butantan Institute,
São Paulo 05503-900, Brazil
6
Department of Pharmacology, Institute of Biomedical Sciences, University of São Paulo,
São Paulo 05508-220, Brazil
* Correspondence: yarac57@gmail.com (Y.C.); vanessa.zambelli@butantan.gov.br(V.O.Z.);
Tel.: +55-11-2627-9765(Y.C. & V.O.Z.)
Abstract: Increased collagen-derived advanced glycation end-products (AGEs) are consistently
related to painful diseases, including osteoarthritis, diabetic neuropathy, and neurodegenerative
disorders. We have recently developed a model combining a two-dimensional glycated extracellular
matrix (ECM-GC) and primary dorsal root ganglion (DRG) that mimicked a pro-nociceptive microen-
vironment. However, culturing primary cells is still a challenge for large-scale screening studies.
Here, we characterized a new model using ECM-GC as a stimulus for human sensory-like neurons
differentiated from SH-SY5Y cell lines to screen for analgesic compounds. First, we confirmed that
the differentiation process induces the expression of neuron markers (MAP2, RBFOX3 (NeuN), and
TUBB3 (β-III tubulin), as well as sensory neuron markers critical for pain sensation (TRPV1, SCN9A
(Nav1.7), SCN10A (Nav1.8), and SCN11A (Nav1.9). Next, we showed that ECM-GC increased c-Fos
expression in human sensory-like neurons, which is suggestive of neuronal activation. In addition,
ECM-GC upregulated the expression of critical genes involved in pain, including SCN9A and TACR1.
Of interest, ECM-GC induced substance P release, a neuropeptide widely involved in neuroinflam-
mation and pain. Finally, morphine, the prototype opiate, decreased ECM-GC-induced substance P
release. Together, our results suggest that we established a functional model that can be useful as a
platform for screening candidates for the management of painful conditions.
Keywords: two-dimensional culture; nociception; inflammatory disease; in vitro assays; analgesic
compounds; high-content screening
1. Introduction
Collagen glycation is frequently observed in neuroinflammatory and neurodegen-
erative disorders, such as Parkinson’s and Alzheimer’s diseases, osteoarthritis, diabetic
neuropathy, amyloid polyneuropathy, and the aging process [1,2]. Glycation is an ir-
reversible and spontaneous process in which proteins, such as collagen, bind to sugar
molecules, forming advanced glycation end products (AGEs) [3]. AGEs can activate spe-
cific cell surface receptors that transduce signals through downstream proteins, leading to
the inflammatory process.
Cells 2022, 11, 247. https://doi.org/10.3390/cells11020247 https://www.mdpi.com/journal/cells