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Natural Flavonoids As Potential Angiotensin-Converting Enzyme 2 Inhibitors for Anti-SARS-Cov-2

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Natural Flavonoids As Potential Angiotensin-Converting Enzyme 2 Inhibitors for Anti-SARS-Cov-2 molecules Review Natural Flavonoids as Potential Angiotensin-Converting Enzyme 2 Inhibitors for Anti-SARS-CoV-2 Muchtaridi Muchtaridi 1,* , M. Fauzi 1, Nur Kusaira Khairul Ikram 2,3 , Amirah Mohd Gazzali 4 and Habibah A. Wahab 5,* 1 Department of Pharmaceutical Analysis and Medicinal Chemistry, Faculty of Pharmacy, Universitas Padjadjaran, Jl Raya 21.5, Bandung-Sumedang 45363, Indonesia; [email protected] 2 Institute of Biological Sciences, Faculty of Science, Universiti Malaya, Kuala Lumpur 50603, Malaysia; [email protected] 3 Centre for Research in Biotechnology for Agriculture (CEBAR), Universiti Malaya, Kuala Lumpur 50603, Malaysia 4 Department of Pharmaceutical Technology, School of Pharmaceutical Sciences, Universiti Sains Malaysia, Gelugor 11800, Penang, Malaysia; [email protected] 5 Pharmaceutical Design and Simulation Laboratory, School of Pharmaceutical Sciences, Universiti Sains Malaysia, Gelugor 11800, Penang, Malaysia * Correspondence: [email protected] (M.M.); [email protected] (H.A.W.); Tel.: +62-22-8784288888 (ext. 3210) (M.M.); +60-4-6532238 (H.A.W.) Received: 3 August 2020; Accepted: 26 August 2020; Published: 1 September 2020 Abstract: Over the years, coronaviruses (CoV) have posed a severe public health threat, causing an increase in mortality and morbidity rates throughout the world. The recent outbreak of a novel coronavirus, named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) caused the current Coronavirus Disease 2019 (COVID-19) pandemic that affected more than 215 countries with over 23 million cases and 800,000 deaths as of today. The situation is critical, especially with the absence of specific medicines or vaccines; hence, efforts toward the development of anti-COVID-19 medicines are being intensively undertaken. One of the potential therapeutic targets of anti-COVID-19 drugs is the angiotensin-converting enzyme 2 (ACE2). ACE2 was identified as a key functional receptor for CoV associated with COVID-19. ACE2, which is located on the surface of the host cells, binds effectively to the spike protein of CoV, thus enabling the virus to infect the epithelial cells of the host. Previous studies showed that certain flavonoids exhibit angiotensin-converting enzyme inhibition activity, which plays a crucial role in the regulation of arterial blood pressure. Thus, it is being postulated that these flavonoids might also interact with ACE2. This postulation might be of interest because these compounds also show antiviral activity in vitro. This article summarizes the natural flavonoids with potential efficacy against COVID-19 through ACE2 receptor inhibition. Keywords: ACE2; COVID-19; flavonoid; coronavirus 1. Introduction Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which is the causative agent of Coronavirus Disease 2019 or COVID-19, triggered a pandemic affecting over 215 countries and territories around the world [1,2]. As of August 2020, there are more than 23 million cases worldwide with over 800,000 deaths, indicating that the virus is highly infectious with its pathogenicity being a global health threat [3–5]. The number of positive cases and deaths due to COVID-19 continues to Molecules 2020, 25, 3980; doi:10.3390/molecules25173980 www.mdpi.com/journal/molecules Molecules 2020, 25, 3980 2 of 20 Molecules 2020, 25, x 2 of 21 increaseincrease rapidly rapidly and, and due, due to to thethe unavailability of of effective effective drug drugs,s, recovery recovery is lagging is lagging (Figure (Figure 1)[2,6,7]1)[. 2,6,7]. Thus, the search for new drugs to overcome this disease needs to be urgently intensified [2,8]. Thus, the search for new drugs to overcome this disease needs to be urgently intensified [2,8]. COVID-19 OVERVIEW 30,000,000 25,000,000 20,000,000 15,000,000 10,000,000 5,000,000 0 Total Corona Virus Cases Corona Virus Total 25-Mar-20 25-Apr-20 25-May-20 25-Jun-20 25-Jul-20 25-Aug-20 25-Mar- 15-May- 15-Jun- 17-Aug- 22-Aug- 28-Aug- 30-Apr 15-Jul-20 20 20 20 20 20 20 Confirmed 426998 3104693 4359294 7800518 13157587 21568480 22536278 24628901 recovered 108578 1054822 1777120 4231240 8057606 14784709 15521145 17094868 Deaths 21985 224447 298287 430424 570450 767028 789197 835689 FigureFigure 1. TheThe rise rise in in active active case casess of coronavirus of coronavirus [2]. [2]. SARS-CoV-2,SARS-CoV-2, which which causes causes severe respiratory respiratory syndrome syndrome in humans in humans,, is a positive is a positive-strand-strand RNA RNA virus.virus. The The virus virus replication replication cyclecycle begins with with the the entry entry of ofthe the virus virus into into the human the human body bodyby attaching by attaching to theto the host host cellular cellular receptorreceptor angiotensin angiotensin-converting-converting enzyme enzyme 2 (ACE2) 2 (ACE2),, assisted assisted by a protein by aspike protein (S), spike (S),followed followed by by the the release release of the of virus the virusgenome genome material material into the host into cell the [9] host. The cellviral [ 9genome]. The contains viral genome containstwo overlapping two overlapping polyproteins polyproteins (polyprotein (polyprotein 1a and polyprotein 1a and 1ab) polyprotein, which are 1ab), cleaved which by Mpro are cleaved (the by Mpromain (the protease) main protease) into 16 non into-structural 16 non-structural proteins, which proteins, are whichthen translated are then into translated structural into (STR structural proteins) and non-structural proteins (non-STRs). This is followed by virus assembly, which releases (STR proteins) and non-structural proteins (non-STRs). This is followed by virus assembly, which virions from the infected cells through exocytosis [10,11]. releasesThe virions angiotensin from the-converting infected enzyme cells through (ACE)- exocytosisrelated carboxypeptidase, [10,11]. ACE2, is a type I integral membraneThe angiotensin-converting protein of 805 amino enzymeacids containing (ACE)-related one HEXXH carboxypeptidase,-E zinc-binding ACE2,consensus is a sequence type I integral membrane[12]. ACE protein2 is involved of 805 aminoin regulating acids containing cardiac function one HEXXH-E and is also zinc-binding a functional consensus receptor sequencefor the [12]. ACE2coronavirus is involved that in causes regulating acute cardiacrespiratory function syndrome and is(SARS). also a ACE functional2 receptors receptor are the for largest the coronavirus target of that causesSARS acute-CoV respiratory-2 because they syndrome play an (SARS).important ACE2 role in receptors the transmission are the largest of virusestarget to alveolar of SARS-CoV-2 cells [13] because. theyInhibition play an importantor regulation role of in ACE the2 transmission receptors may of potentially viruses to alveolarbe effective cells in [the13]. treatment Inhibition of orCOVID regulation- of ACE219. receptorsCOVID-19 may is currently potentially being be effective treated inwith the anti treatment-infective of COVID-19.drugs such COVID-19as antimalarial is currently drugs being treated(chloroquine, with anti-infective hydroxychloroquine drugs such [14 as- antimalarial17], antiviral drugs drugs (chloroquine, (remdesivir hydroxychloroquine[18], saquinavir [19][, 14–17], favipiravir [20], lopinavir [21], ribavirin [22], and oseltamivir), and certain immunosuppressive drugs antiviral drugs (remdesivir [18], saquinavir [19], favipiravir [20], lopinavir [21], ribavirin [22], such as tocilizumab [23]. Tocilizumab was approved by the Food and Drug Administration (FDA) to andmanage oseltamivir), cytokine and release certain syndrome immunosuppressive (CRS) in patients drugs receiving such aschimeric tocilizumab antigen [23 receptor]. Tocilizumab T-cell was approvedtherapy. by This the Fooddrug was and Drugshown Administration to reduce toxicity (FDA) and toimprove manage immune cytokine-related release toxicity syndrome [24,25] (CRS). in patientsTocilizumab receiving can chimericblock the activity antigen of receptor proinflammatory T-cell therapy. interleukin This-6 drug(IL-6), was which shown is involved to reduce in the toxicity andpathogenesis improve immune-related of pneumonia that toxicity causes [24 death,25]. in Tocilizumab COVID-19 patients can block [26] the. However, activity to of date, proinflammatory we are interleukin-6still waiting (IL-6), for the whichresults of is the involved ongoing in phase the pathogenesis3 clinical trial that of pneumoniamight support that and causes prove the death in COVID-19effectiveness patients of these [26 ].drugs However, in treating to date,patients we with are stillSARS waiting-CoV-2 infection for the results. For example, of the Wang ongoing et al phase. 3 clinical(2020 trial) conducted that might a randomized support andstudy prove on the the use e ffofectiveness placebo-controlled of these and drugs intravenous in treating remdesivir patients with SARS-CoV-2 infection. For example, Wang et al. (2020) conducted a randomized study on the use of placebo-controlled and intravenous remdesivir in 10 hospitals in Hubei, China [27]. The study found that intravenous remdesivir did not significantly increase the time for clinical improvement, Molecules 2020, 25, 3980 3 of 20 the mortality, or the time for virus clearance in patients with serious SARS-CoV-2 compared to placebo. However, hydroxychloroquine or chloroquine with or without azithromycin did not enhance clinical status at 15 days [28]. In an effort to find new therapies for COVID-19, natural product sources are also being explored and re-evaluated for their activity against this
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