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Type III Secretion Effectors with Arginine N-Glycosyltransferase

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Type III Secretion Effectors with Arginine N-Glycosyltransferase microorganisms Review Type III Secretion Effectors with Arginine N-Glycosyltransferase Activity Juan Luis Araujo-Garrido, Joaquín Bernal-Bayard and Francisco Ramos-Morales * Departamento de Genética, Facultad de Biología, Universidad de Sevilla, 41012 Sevilla, Spain; [email protected] (J.L.A.-G.); [email protected] (J.B.-B.) * Correspondence: [email protected] Received: 12 February 2020; Accepted: 29 February 2020; Published: 2 March 2020 Abstract: Type III secretion systems are used by many Gram-negative bacterial pathogens to inject proteins, known as effectors, into the cytosol of host cells. These virulence factors interfere with a diverse array of host signal transduction pathways and cellular processes. Many effectors have catalytic activities to promote post-translational modifications of host proteins. This review focuses on a family of effectors with glycosyltransferase activity that catalyze addition of N-acetyl-d-glucosamine to specific arginine residues in target proteins, leading to reduced NF-κB pathway activation and impaired host cell death. This family includes NleB from Citrobacter rodentium, NleB1 and NleB2 from enteropathogenic and enterohemorrhagic Escherichia coli, and SseK1, SseK2, and SseK3 from Salmonella enterica. First, we place these effectors in the general framework of the glycosyltransferase superfamily and in the particular context of the role of glycosylation in bacterial pathogenesis. Then, we provide detailed information about currently known members of this family, their role in virulence, and their targets. Keywords: glycosyltransferases; type III secretion; effectors; NleB; SseK; Citrobacter; Escherichia; Salmonella; death domains 1. Introduction Type III secretion systems (T3SSs) are fundamental tools for the interaction between many pathogenic and symbiotic Gram-negative bacteria and their hosts. T3SSs, also known as injectisomes, span the bacterial inner and outer membranes and form injection nanomachines that deliver proteins, known as effectors, into target eukaryotic cells to modulate a variety of cellular functions [1,2]. Effectors have diverse activities and targets, and typically have an N-terminal secretion domain and one or more C-terminal functional domains [3,4]. Effectors can be classified in four non-mutually exclusive categories according to their mechanisms of activity [5]: (i) effectors that mediate their activities through physical interactions with host targets; (ii) effectors that use functional or structural mimicry to alter host cell processes; (iii) effectors that promote post-translational modifications of host proteins; and (iv) effectors with protease activity. Examples of catalytic activities of effectors are ubiquitination, deubiquitination, phosphorylation, dephosphorylation, acetylation, deamidation, ADP ribosylation, cysteine methylation, and glycosylation. This review focuses on a specific family of T3SS effectors with glycosyltransferase activity that are found in Salmonella enterica and in attaching/effacing (A/E) pathogens. Salmonellae are facultative intracellular Gram-negative bacterial pathogens belonging to the family Enterobacteriaceae. The genus Salmonella includes the species S. bongori and S. enterica, the latter divided into six subspecies and more than 2500 serovars [6]. S. enterica possesses two virulence-related T3SS [7–9], T3SS1 and T3SS2, that are encoded by Salmonella pathogenicity island 1 (SPI1) and Salmonella pathogenicity island 2 (SPI2) (Figure1), respectively, whereas S. bongori lacks SPI2 [10]. The T3SS1 translocates effectors across the host cell plasma membrane that promote Salmonella Microorganisms 2020, 8, 357; doi:10.3390/microorganisms8030357 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 357 2 of 24 invasionMicroorganisms into epithelial 2020, 8, cells357 in the intestine and stimulate localized inflammation [11]. The2 of 23 T3SS2 is expressedThe intracellularly T3SS1 translocates in responseeffectors across to acidic the host pH andcell plasma nutrient membrane limitation that found promote in theSalmonella lumen of the Salmonellainvasion-containing into epithelial vacuole cells (SCV), in the a intestine modified and phagolysosome stimulate localized which inflammation is the typical [11]. The intracellular T3SS2 is niche of this pathogenexpressed intracellularly [12]. T3SS2 e inff ectorsresponse are to translocatedacidic pH and throughnutrient limitation the SCV found membrane, in the lumen are importantof the in intestinalSalmonella and disseminated‐containing vacuole infections, (SCV), and a modified are required phagolysosome for growth which within is the diff typicalerent hostintracellular cell types [13]. niche of this pathogen [12]. T3SS2 effectors are translocated through the SCV membrane, are Together, T3SS1 and T3SS2 secrete more than 40 effectors, some encoded by SPI1 or SPI2, but most important in intestinal and disseminated infections, and are required for growth within different host encodedcell outside types [13]. these Together, islands, T3SS1 in other and T3SS2 horizontally secrete more acquired than 40 regions effectors, of some the genome encoded by [14 SPI1–17 ].or EnterohemorrhagicSPI2, but most encodedEscherichia outside these coli (EHEC) islands, in and other enteropathogenic horizontally acquiredE. coli regions(EPEC) of the are genome extracellular human pathogens[14–17]. that attach to the intestinal epithelium and efface brush border microvilli forming A/E lesions [Enterohemorrhagic18]. EHEC causes Escherichia hemorrhagic coli (EHEC) colitis and and enteropathogenic hemolytic uremic E. coli (EPEC) syndrome, are extracellular whereas EPEC is a causehuman of infantile pathogens diarrhea. that attachCitrobacter to the intestinal rodentium epitheliumis another and efface A /brushE pathogen border microvilli which is forming the causative A/E lesions [18]. EHEC causes hemorrhagic colitis and hemolytic uremic syndrome, whereas EPEC C. rodentium agent ofis murine a cause of transmissible infantile diarrhea. colonic Citrobacter hyperplasia rodentium [19 is ].another Lesions A/E induced pathogen by which is the causativein mice are similar toagent those of murine caused transmissible by EHEC or colonic EPEC hyperplasia in humans [19]. and Lesions these induced pathogens by C. share rodentium a number in mice of are virulence determinantssimilar includingto those caused the locusby EHEC of enterocyteor EPEC in ehumansffacement and (LEE)these pathogens [20,21] (Figure share a1 ).number The LEEof is a 34 kb pathogenicityvirulence determinants island with including 41 genes the locus that of encodeenterocyte all effacement the structural (LEE) [20,21] components (Figure 1). of The a T3SS, LEE seven of its effisectors a 34 kb and pathogenicity their chaperones, island with proteins 41 genes involvedthat encode in all adherence, the structural and components regulatory of a proteins T3SS, [22]. seven of its effectors and their chaperones, proteins involved in adherence, and regulatory proteins Many effectors are encoded outside the LEE, and the total number of effectors is at least 29 in C. [22]. Many effectors are encoded outside the LEE, and the total number of effectors is at least 29 in C. rodentiumrodentium, 22 in, EPEC,22 in EPEC, and and 39 39 in in EHEC EHEC [22]. [22]. A Asecond second gene gene cluster, cluster, potentially potentially encoding encodinga T3SS and a T3SS and knownknown as as ETT2, ETT2, for forE. E. coli coli T3SST3SS 2, is present present in in many many E. E.coli coli strainsstrains [23,24]. [23 ,ETT224]. ETT2resembles resembles the the SalmonellaSalmonellaT3SS1 butT3SS1 in mostbut in cases most itcases has it been has subjectedbeen subjected to mutational to mutational attrition attrition and and there there is is no no evidence for the secretionevidence for of etheffectors secretion by thisof effectors system by [25 this]. However,system [25]. this However, region this is intact region in is some intact strains in some of E. coli and Escherichiastrains of albertii E. coli ,and and Escherichia appears albertii to be, importantand appears for to be bacterial important pathogenesis for bacterial pathogenesis [25–27]. [25– 27]. Figure 1.FigureGenetic 1. Genetic structure structure of Salmonella of Salmonellapathogenicity pathogenicity island island 1 (SPI1) 1 (SPI1) and and SalmonellaSalmonella pathogenicitypathogenicity island 2 (SPI2) of S. enterica serovar Typhimurium strain 14028, and the locus of enterocyte effacement island 2 (SPI2) of S. enterica serovar Typhimurium strain 14028, and the locus of enterocyte effacement (LEE) island of E. coli O127:H6 strain E2348/69. Genes are colored according to their functional (LEE) islandcategories of E.[22,28]. coli O127:H6 strain E2348/69. Genes are colored according to their functional categories [22,28]. 2. Glycosyltransferases Glycosyltransferases (GTs) catalyze the formation of glycoside bonds using an activated donor sugar substrate that contains a nucleoside phosphate or a lipid phosphate leaving group [29]. Enzymes that use sugar mono- or diphosphonucleotides as donors are known as Leloir GTs [30]. Microorganisms 2020, 8, 357 3 of 23 2. Glycosyltransferases Glycosyltransferases (GTs) catalyze the formation of glycoside bonds using an activated donor sugar substrate that contains a nucleoside phosphate or a lipid phosphate leaving group [29]. Enzymes that use sugar mono‐ or diphosphonucleotides as donors are known as Leloir GTs [30]. NonMicroorganisms‐Leloir GTs2020 , 8use, 357 non‐nucleotide donors, such as polyprenol pyrophosphates, polyprenol3 of 24 phosphates,
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