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Promising Antioxidant Activity of Erythrina Genus: an Alternative Treatment for Inflammatory Pain?

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Promising Antioxidant Activity of Erythrina Genus: an Alternative Treatment for Inflammatory Pain? International Journal of Molecular Sciences Review Promising Antioxidant Activity of Erythrina Genus: An Alternative Treatment for Inflammatory Pain? Tania Jiménez-Cabrera 1 , Mirandeli Bautista 1,* , Claudia Velázquez-González 1, Osmar Antonio Jaramillo-Morales 2 , José Antonio Guerrero-Solano 1 , Thania Alejandra Urrutia-Hernández 1 and Minarda De la O-Arciniega 1,* 1 Institute of Health Sciences, Autonomous University of the State of Hidalgo, San Agustin Tlaxiaca 55679, Hidalgo, Mexico; [email protected] (T.J.-C.); [email protected] (C.V.-G.); [email protected] (J.A.G.-S.); [email protected] (T.A.U.-H.) 2 Nursing and Obstetrics Department, Life Sciences Division, Campus Irapuato-Salamanca, Ex Hacienda El Copal, Km. 9 Carretera Irapuato-Silao, A.P 311, Irapuato 36500, Guanajuato, Mexico; [email protected] * Correspondence: [email protected] (M.B.); [email protected] (M.D.l.O.-A.) Abstract: The negative impact that oxidative stress has on health is currently known. The complex mechanism of free radicals initiates a series of chain reactions that contribute to the evolution or development of different degenerative disorders. Likewise, these disorders are usually accompanied by inflammatory processes and, therefore, pain. In this sense, reactive oxygen species (ROS) have been shown to promote the nociceptive process, but effective treatment of pain and inflammation still represents a challenge. Over time, it has been learned that there is no single way to relieve pain, and as long as there are no other alternatives, the trend will continue to apply multidisciplinary management, such as promote the traditional use of the Erythrina genus to manage pain and inflammation. In this sense, the Erythrina genus produces a wide range of secondary metabolites, including flavanones, isoflavones, isoflavones, and pterocarpans; these compounds are characterized by their antioxidant activity. Phenolic compounds have demonstrated their ability to suppress pro-oxidants and inhibit Citation: Jiménez-Cabrera, T.; Bautista, inflammatory signaling pathways such as MAPK, AP1, and NFκB. Although there is preclinical M.; Velázquez-González, C.; Jaramillo- evidence supporting its use, the pharmacological effect mechanisms are not entirely clear. Nowadays, Morales, O.A.; Guerrero-Solano, J.A.; there is a fast advancement in knowledge of the disciplines related to drug discovery, but most of Urrutia-Hernández, T.A.; De la nature’s medicinal potential has not yet been harnessed. This review analyzes the decisive role that O-Arciniega, M. Promising Antioxidant the Erythrina genus could play in managing inflammatory pain mediated by its compounds and its Activity of Erythrina Genus: An uses as an antioxidant. Alternative Treatment for Inflammatory Pain? Int. J. Mol. Sci. 2021, 22, 248. Keywords: Erythrina; antioxidant; inflammatory pain; prenylated flavonoids https://doi.org/10.3390/ijms22010248 Received: 20 November 2020 Accepted: 23 December 2020 Published: 29 December 2020 1. Molecular Origin of Inflammatory Pain Pain is traditionally defined as a complex sensory and emotional experience associated Publisher’s Note: MDPI stays neu- with actual or potential tissue damage or described in terms of such damage (International tral with regard to jurisdictional claims Association for the Study of Pain) [1–3]. It is a complex process that involves neuronal in published maps and institutional signaling pathways between the peripheral nervous system (PNS) and the central nervous affiliations. system (CNS) [1,3]. The transduction of noxious stimuli (those that actually or potentially damage tissues) is carried out by a nociceptor, creating an electrophysiological neuronal signal encoded in the form of an action potential that is transmitted to the CNS. The acute Copyright: © 2020 by the authors. Li- injury is associated with a first, well-localized pain sensation transduced and transmitted by censee MDPI, Basel, Switzerland. This nociceptors. Although pain is one of the body’s most important adaptation and protection article is an open access article distributed mechanisms, the degree of tissue damage leads to the release of inflammatory mediators under the terms and conditions of the that bind to its receptors, triggering an enzymatic cascade [1]. Thus, inflammatory pain is Creative Commons Attribution (CC BY) generated by an increase in sensitivity due to the cellular response associated with tissue license (https://creativecommons.org/ damage, promoting the influx of activated cells such as macrophages, lymphocytes, and licenses/by/4.0/). mast cells that release inflammatory mediators such as bradykinin, Hþ ions, ATP, purines, Int. J. Mol. Sci. 2021, 22, 248. https://doi.org/10.3390/ijms22010248 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 20 Int. J. Mol. Sci. 2021, 22, 248 2 of 19 rophages, lymphocytes, and mast cells that release inflammatory mediators such as brad- ykinin, Hþ ions, ATP, purines, prostaglandin E2, leukotrienes, cytokines, nerve growth prostaglandinfactor (NGF), sympathetic E2, leukotrienes, amines, cytokines, and oxidative nerve growth stress products factor (NGF), present sympathetic in the membrane amines, andof nociceptors oxidative stress[4] (Figure products 1). NGF present released in the by membrane activated ofmacrophages nociceptors acts [4] (Figuredirectly1 ).on NGF pep- releasedtidergic C by fibers activated that express macrophages the TrkA acts receptor, directly a on key peptidergic component C of fibers peripheral that express sensitiza- the TrkAtion. receptor,Macrophages a key release component cytokines of peripheral such as sensitization. interleukin-6 Macrophages (IL-6), IL-1b, release tumor cytokines necrosis suchfactor as α interleukin-6 (TNFα) which (IL-6), in turn IL-1b, contribute tumor necrosis to peripheral factor α (TNFsensitizationα) which through in turn contribute increased tolocal peripheral production sensitization of proalgesic through agents increased such as local bradykinin, production prostaglandins of proalgesic agentsand increased such as bradykinin,release of NGF prostaglandins [1]. Prostaglandins and increased are synthesized release of by NGF consecutive [1]. Prostaglandins reactions initiated are synthe- by sizedthe phospholipase by consecutive A2 reactions enzyme initiatedthat causes by thethe phospholipaserelease of arachidonic A2 enzyme acid that(AA) causes from thecell releasemembranes. of arachidonic Cyclooxygenase-2 acid (AA) (COX2) from cell metabolizes membranes. arachidonic Cyclooxygenase-2 acid to prostaglandin (COX2) metabo- G2 lizes(PGG2) arachidonic and prostaglandin acid to prostaglandin H2 (PGH2) G2which (PGG2) is ultimately and prostaglandin converted H2 to (PGH2)PGE2 by which prosta- is ultimatelyglandin E synthase converted (PTGES) to PGE2 [5]. by PGE2 prostaglandin acts on all Efour synthase E-prostanoid (PTGES) (EP) [5]. receptor PGE2 acts subtypes on all four(EP1-4). E-prostanoid In peripheral (EP) tissue, receptor PGE2 subtypes modulates (EP1-4). pain In sensitivity peripheral by tissue, sensitizing PGE2 primary modulates af- painferents. sensitivity Sensitizes by sensitizingion channels primary involved afferents. in pain, Sensitizes namely ion transient channels receptor involved potential in pain, namelyvanilloid transient 1 channel, receptor tetrodotoxin-sensitive potential vanilloid Na+ 1 channel, channels, tetrodotoxin-sensitive and purinergic P2X3 Na+ channels, chan- nels,also enhances and purinergic the release P2X3 channels,of neurotransmitters. also enhances So, the it releaseis a crucial of neurotransmitters. lipid mediator of So,inflam- it is amatory crucial responses lipid mediator that causes of inflammatory pain hypersensitivity responses that [6]. causes pain hypersensitivity [6]. FigureFigure 1.1. Diagram ofof thethe processprocess ofof painpain andand peripheralperipheral sensitizationsensitization leadingleading to to inflammatory inflammatory pain. pain. The pathological effects of ROS, IL-1β, TNFα, and IL-6 are due to the activation of variousThe pro-inflammatory pathological effects signaling of ROS, pathways IL-1β, TNF includingα, and IL-6 the are three due (ERK, to the JNK, activation and p38) of mitogen-activatedvarious pro-inflammatory protein kinasessignaling (MAPK), pathways NF κincludingB, AP1, and the JAK/STATthree (ERK, [7 JNK,]. There and is p38) evi- dencemitogen-activated that mitochondrial protein dysfunction kinases (MAPK), induced NF byκB, oxidative AP1, and and JAK/STAT nitrosative [7]. stress There leads is evi- to peripheraldence that andmitochondrial central sensitization. dysfunction Mammalian induced bynerves oxidative are and especially nitrosative susceptible stress leads to free to radicals,peripheral both and oxygen central (ROS) sensitization. and nitrogen Mammalian (RNS), due nerves to the are high especially content susceptible of phospholipids to free andradicals, axonal both mitochondria; oxygen (ROS) in and addition nitrogen to (RNS), having due a weak to the antioxidant high content system of phospholipids and other hand,and axonal some studiesmitochondria; on antioxidant in addition supplementation to having a inweak animal antioxidant models show system that and hydroxyl other − radicalshand, some (OH), studies superoxide on antioxidant (O2 ), and supplementati nitric oxide (ON)on in mayanimal have models a role show in peripheral that hydroxyl sensi- tizationradicals due(OH), to superoxide a deleterious (O effect2−), and on nitric lipids oxide and nucleic (ON)
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