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Unique Features of Entamoeba Sulfur Metabolism; Compartmentalization, Physiological Roles of Terminal Products, Evolution and Pharmaceutical Exploitation

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International Journal of Molecular Sciences Review Unique Features of Entamoeba Sulfur Metabolism; Compartmentalization, Physiological Roles of Terminal Products, Evolution and Pharmaceutical Exploitation Fumika Mi-ichi * and Hiroki Yoshida Division of Molecular and Cellular Immunoscience, Department of Biomolecular Sciences, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga 849-8501, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-952-34-2294 Received: 30 August 2019; Accepted: 19 September 2019; Published: 21 September 2019 Abstract: Sulfur metabolism is essential for all living organisms. Recently, unique features of the Entamoeba metabolic pathway for sulfated biomolecules have been described. Entamoeba is a genus in the phylum Amoebozoa and includes the causative agent for amoebiasis, a global public health problem. This review gives an overview of the general features of the synthesis and degradation of sulfated biomolecules, and then highlights the characteristics that are unique to Entamoeba. Future biological and pharmaceutical perspectives are also discussed. Keywords: amoebiasis; mitosome; lipid metabolism; encystation; lateral gene transfer 1. Introduction 1.1. Sulfur Metabolism Sulfur is an essential element for life in all living organisms. Sulfate in the environment is typically activated as a prerequisite step for both sulfation and sulfate assimilation pathways. Sulfate activation is broadly found throughout the Bacteria, Protista, Fungi, Plantae, and Metazoa kingdoms [1,2]; KEGG (see Box1). Box 1. Databases. Sulfur metabolism research has greatly benefited from ever-expanding databases, such as the Kyoto Encyclopedia of Genes and Genomes (KEGG) (https://www.genome.jp/kegg/), The National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/), and AmoebaDB (https://amoebadb.org/ amoeba/). The information available in such databases is, therefore, cited in this review where necessary. Sulfate taken up from the external milieu is activated by two sequential reactions to provide adenosine 50-phosphosulfate (APS) and 30-phosphoadenosine 50-phosphosulfate (PAPS), respectively. PAPS then acts as a sulfate donor in a sulfotransferase (SULT) reaction, in which sulfate is transferred to a variety of acceptors, to generate sulfated sugars, proteins, lipids, glycolipids and small organic molecules [3,4]. The various products generated are often hydrolyzed by sulfatase (SF) [4,5]. Meanwhile, some organisms, such as plants, APS and PAPS, serve as intermediates in branched pathways and in sulfate assimilation pathways for synthesizing a wide array of sulfur-containing biomolecules crucial for living organisms, such as thiol-containing amino acids (cysteine and methionine) and sulfur-containing cofactors (Fe-S clusters, thiamine, and coenzyme A (CoA)) [2–4]. An overview of the metabolic pathways that are functionally linked to sulfate activation is illustrated in Figure1. Int. J. Mol. Sci. 2019, 20, 4679; doi:10.3390/ijms20194679 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 13 (CoA)) [2–4]. An overview of the metabolic pathways that are functionally linked to sulfate Int. J. Mol. Sci. 2019, 20, 4679 2 of 13 activation is illustrated in Figure 1. Figure 1. Overview of sulfate metabolism functionally linked to sulfate activation. An overall Figure 1. Overview of sulfate metabolism functionally linked to sulfate activation. An overall metabolic pathway is depicted, in which information from bacterial to human studies is integrated. metabolicNote that pathwayEntamoeba isdoes depicted, not possess in which genes information encoding APS from and bacterial PAPS reductases to human (AmoebaDB; studies is integrated. KEGG). NoteThe enzymethat Entamoeba responsible does for not each possess step is showngenes byencoding a filled oval. APS Abbreviations and PAPS reductases used: APS, (AmoebaDB; adenosine KEGG).50-phosphosulfate; The enzyme APSK, responsible APS kinase; for each AS, step ATP is sulfurylase; shown by IPP,a filled inorganic oval. Abbreviations pyrophosphatase; used: PAP, APS, adenosineadenosine 350,5′-phosphosulfate;0-bisphosphate; PAPase, APSK, 30(2 0),5APS0-bisphosphate kinase; AS, nucleotidase; ATP sulfurylase; PAPS, 30-phosphoadenosine IPP, inorganic pyrophosphatase;50-phosphosulfate; PAP, Pi, inorganic adenosine phosphate; 3′,5′-bisphosphate; PPi, inorganic PAPase, pyrophosphate; 3′(2′),5′-bisphosphate SF, sulfatase; nucleotidase; and SULT, PAPS,sulfotransferase. 3′-phosphoadenosine Enzymatic reactions5′-phosphosulfate; are indicated Pi, by arrows.inorganic Multiple phosphate; steps for PPi, synthesizing inorganic pyrophosphate;sulfur-containing SF, biomolecules sulfatase; an isd simplified SULT, sulfotransferase. by dashed arrow. Enzymatic Fine dotted reactions lines indicate are indicated molecular by arrows.transfer Multiple of APS and steps PAPS. for synthesizing sulfur-containing biomolecules is simplified by dashed arrow. Fine dotted lines indicate molecular transfer of APS and PAPS. 1.2. Entamoeba Histolytica Infection Causes Amoebiasis 1.2. EntamoebaE. histolytica Histolyticabelongs Infection to the phylum Causes AmoebozoaAmoebiasis in the kingdom Protista. E. histolytica infection causes amoebiasis, a parasitic disease that is prevalent worldwide [6–9]. The infection usually occurs by theE. histolytica oral ingestion belongs of cysts. to the The phylum ingested Amoebozoa cysts then travel in the to thekingdom small intestine Protista. where E. histolytica they hatch infection into causestrophozoites. amoebiasis, Trophozoites a parasitic then disease descend that to is the prevalent large intestine worldwide and proliferate [6–9]. The there. infection Some proliferatingusually occurs bytrophozoites the oral ingestion invade of the cysts. mucosal The tissue ingested and cysts can be then transported travel to via the the small blood intestine stream towhere other they organs hatch intoapart trophozoites. from the intestine Trophozoites wherethey then can descend form abscesses, to the large most intestine commonly and in theproliferate liver. Meanwhile, there. Some proliferatingsome trophozoites trophozoites in the invade large intestine the mucosal differentiate tissue and into can dormant be transported cysts, which via arethe thenblood excreted stream to otherin feces organs (Figure apart2)[ from10]. the The intestine water or where food contaminated they can form by abscesses, feces from most infected commonly individuals in the is theliver. Meanwhile,principal source some oftrophozoites amoebiasis in [8 ,the9]. Therefore,large intestine the parasiticdifferentiate life cycle into dorman of E. histolyticat cysts, iswhich essentially are then excretedmaintained in feces by alternating (Figure 2) its [10]. proliferative The water trophozoite or food contaminated and dormant by cyst feces forms. from The infected proliferative individuals and is invasivethe principal capabilities source of trophozoites of amoebiasis cause [8,9]. typical Therefore, amoebiasis the symptoms, parasitic such life as cycle dysentery of E. and histolytica hepatic is essentiallyabscess. Meanwhile, maintained disease by alternating transmission its requiresproliferative the dormancy trophozoite of cysts and and dormant the high cyst occurrence forms. ofThe proliferativeasymptomatic and patients invasive who capabilities unconsciously of trophozoites spread the disease cause typical is a serious amoebiasis public health symptoms, problem such [9]. as dysenteryCurrent clinicaland hepatic options abscess. are inadequate. Meanwhile, Available disease drugs transmission are limited requires and an the effective dormancy vaccine of hascysts not and the high occurrence of asymptomatic patients who unconsciously spread the disease is a serious public health problem [9]. Current clinical options are inadequate. Available drugs are limited and Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 3 of 13 Int. J. Mol. Sci. 2019, 20, 4679 3 of 13 an effective vaccine has not been developed [6,8]. Hence, new measures for killing trophozoites and halting cyst formation, such as anti-amoebic and amoebiasis transmission-blocking drugs, are beenurgently developed needed. [6 ,8]. Hence, new measures for killing trophozoites and halting cyst formation, such as anti-amoebic and amoebiasis transmission-blocking drugs, are urgently needed. Figure 2. Entamoeba histolytica, the causative agent for amoebiasis. Schematic illustration of the main Figure 2. Entamoeba histolytica, the causative agent for amoebiasis. Schematic illustration of the main route of infection and behavior inside the human host is shown. The life cycle of E. histolytica essentially route of infection and behavior inside the human host is shown. The life cycle of E. histolytica consists of proliferative trophozoite and dormant cyst stages. essentially consists of proliferative trophozoite and dormant cyst stages. This review focuses on Entamoeba sulfur metabolism and highlights its unique features of spatial compartmentalization,This review focuses the on terminal Entamoeba products sulfur produced metabolism and theirand roleshighlights in physiology its unique and features evolution. of Entamoebaspatial compartmentalization,sulfur metabolism from the pharmaceuticalterminal produc andts produced biological perspectivesand their roles isalso in physiology discussed. and evolution. Entamoeba sulfur metabolism from pharmaceutical and biological perspectives is also 2.discussed. Biosynthesis and
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