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The Example of Neisseria Meningitidis. Cyril Guilhen, Muhamed-Kheir Taha, Frédéric Veyrier

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The Example of Neisseria Meningitidis. Cyril Guilhen, Muhamed-Kheir Taha, Frédéric Veyrier Role of transition metal exporters in virulence: the example of Neisseria meningitidis. Cyril Guilhen, Muhamed-Kheir Taha, Frédéric Veyrier To cite this version: Cyril Guilhen, Muhamed-Kheir Taha, Frédéric Veyrier. Role of transition metal exporters in virulence: the example of Neisseria meningitidis.. Frontiers in Cellular and Infection Microbiology, Frontiers, 2013, 3, pp.102. 10.3389/fcimb.2013.00102. pasteur-02093303 HAL Id: pasteur-02093303 https://hal-pasteur.archives-ouvertes.fr/pasteur-02093303 Submitted on 8 Apr 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License PERSPECTIVE ARTICLE published: 23 December 2013 CELLULAR AND INFECTION MICROBIOLOGY doi: 10.3389/fcimb.2013.00102 Role of transition metal exporters in virulence: the example of Neisseria meningitidis Cyril Guilhen , Muhamed-Kheir Taha and Frédéric J. Veyrier* Département Infection et Epidémiologie, Institut Pasteur, Unité des Infections Bactériennes Invasives, Paris, France Edited by: Transition metals such as iron, manganese, and zinc are essential micronutrients for Mathieu F.Cellier, Institut National bacteria. However, at high concentration, they can generate non-functional proteins de la Recherche Scientifique, or toxic compounds. Metal metabolism is therefore regulated to prevent shortage or Canada overload, both of which can impair cell survival. In addition, equilibrium among these Reviewed by: Caroline Genco, Boston University metals has to be tightly controlled to avoid molecular replacement in the active site School of Medicine, USA of enzymes. Bacteria must actively maintain intracellular metal concentrations to meet Thomas Kehl-Fie, University of physiological needs within the context of the local environment. When intracellular Illinois, USA buffering capacity is reached, they rely primarily on membrane-localized exporters to *Correspondence: maintain metal homeostasis. Recently, several groups have characterized new export Frédéric J. Veyrier, Département Infection et Epidémiologie, Institut systems and emphasized their importance in the virulence of several pathogens. Pasteur, Unité des Infections This article discusses the role of export systems as general virulence determinants. Bactériennes Invasives, 28 Rue du Furthermore, it highlights the contribution of these exporters in pathogens emergence Dr. Roux, 75015 Paris, France with emphasis on the human nasopharyngeal colonizer Neisseria meningitidis. e-mail: [email protected] Keywords: virulence factors, Neisseria meningitidis, metals, exporter, efflux INTRODUCTION to call attention to these efflux systems as virulence factors, For decades, it has been known that transition metals played a as they have received less attention than metal importer sys- role in regulating host pathogen relationships (Weinberg, 1971; tems. This article offers a brief perspective of the different Finkelstein et al., 1983). Bacterial pathogens must acquire these families of metallo-exporters and a discussion of their general metals in order to survive in the host during an infection. Metals importance in the virulence of bacterial pathogens with empha- such as Fe, Mn, Zn, Ni, Cu, Co, and Mo (Schaible and Kaufmann, sis on Neisseria meningitidis,anobligatehumanrespiratory 2005) have an incomplete “d” orbital which permits different symbiont. states of oxidation, e.g., Fe2+ and Fe3+. These metals often serve essential roles in protein structural stabilization or as enzymes METAL EFFLUX SYSTEMS cofactors (Barondeau and Getzoff, 2004). However, the unique The concentrations of metals can vary dramatically in the chemistry of these metals can also provoke inappropriate redox host organism during the course of a bacterial infection, and − reactions with O2 and H2O2, (Fenton’s reaction), generating pathogens have developed a large panel of exporters to regu- highly damaging hydroxyl radicals (OH and OH−) that can ulti- late their intracellular metal concentrations. Currently five main mately lead to the cell death (Stadtman, 1990). It is perhaps this classes of bacterial exporters (Figure 1) have been described: duality that has driven the selection of sophisticated bacterial strategies to orchestrate transition metal homeostasis by sensing, 1. The Resistance-Nodulation-Cell division (RND) type trans- acquiring, storing, or when necessary, exporting these essential porters are integral membrane proteins mediating the efflux but potentially lethal metals. of a broad variety of substrates with a subset exporting metals. The stringent and complex requirements of bacterial This subgroup is named heavy-metal efflux RND (HME- pathogens for metals have been exploited by the immune system RND). This tripartite transporter utilizes the proton motive to limit bacterial growth. The majority of described examples force to drive the efflux of the substrates (Nies, 1995; Goldberg demonstrate that the immune system uses starvation strategies et al., 1999). The RND pump (annotated A in Figure 1)is + + that consist in decreasing metal availability (mainly Fe2 ,Zn2 , an integral membrane protein with a hydrophilic periplas- + and Mn2 )(Canonne-Hergaux et al., 1999; Corbin et al., 2008) mic component, connected to a trimeric outer membrane to restrict bacterial growth. However, recent reports suggest factor (C in Figure 1). This outer membrane channel allows the existence of an immune strategy whereby the bacteria are the efflux of metal into the extracellular space (Paulsen et al., + poisoned with an overload of metal, principally Zn2 and 1997). The third part of the RND transporter complex is com- +/ + Cu 2 (White et al., 2009). This latter finding also corrob- posed of several units of a periplasmic membrane protein (B in orates the fact that deletion of bacterial efflux pumps often Figure 1). It serves as an adaptor that forms a ring around the impairs the virulence of pathogens (Stahler et al., 2006; Rosch outer membrane proteins and the pump, thereby stabilizing et al., 2009; Botella et al., 2011; Li et al., 2011; Veyrier et al., contact between the two other components (Murakami et al., 2011; Padilla-Benavides et al., 2013). It is therefore important 2002; Akama et al., 2004a,b). Frontiers in Cellular and Infection Microbiology www.frontiersin.org December 2013 | Volume 3 | Article 102 | 1 Guilhen et al. Metallo-exporters as virulence factors FIGURE 1 | The different families of metal exporters. The different families (Transporter Mediating Manganese Export) family, and the CorA family of metal exporters include the Resistance-Nodulation-Cell division (RND) type (Cobalt Resistance protein A). As schematized by a question-mark, the transporters, the P-type ATPase family (forming a covalent phosphorylated subsequent export from the periplasm to the extracellular space can be intermediate), the Cation Diffusion Facilitator (CDF) family, the MntX mediated via an unknown porin or passively. Several RND exporter systems have been identified to date, transport various metals in both prokaryotes and eukaryotes including CzcABC from Cupriavidus metallidurans which (Haney et al., 2005). The first description of a CDF protein mediates the efflux of Co2+,Zn2+,andCd2+ with different was YiiP from E. coli and its function, the efflux of Cd2+ and affinities. The deletion of czcC (the outer membrane com- Zn2+,iscoupledtoH+ antiport. In addition, Fe2+ was also ponent) resulted in a decrease of Cd2+ and Co2+ efflux suggested to be exported through YiiP (Grass et al., 2005) whereas the lack of czcA or czcB, the pump and fusion pro- but subsequent studies have shown that Fe2+ transport is not tein, respectively, induced a complete loss of efflux activity as efficient as for Cd2+ and Zn2+ (Wei and Fu, 2005; Hoch (Nies and Silver, 1989; Nies et al., 1989; Goldberg et al., et al., 2012). YiiP and other members of the family are usu- 1999). Other characterized RND systems include CnrABC ally composed of six transmembrane domains followed by from Alcaligenes eutrophus which mediates the efflux of Co2+ a metallochaperone-like cytoplasmic domain that regulates and Ni2+ (Liesegang et al., 1993), CznABC from Helicobacter metal transport activity (Lu et al., 2009). Crystal structures pylori which mediates resistance against high concentrations revealed an inward-facing homodimeric structure with four of Ni2+,Zn2+,andCd2+ (Stahler et al., 2006)andCusABC Zn2+ binding sites per monomer, designated Z1–Z4 (Lu and from E. coli which mediates the efflux of Cu+ and Ag+ (Long Fu, 2007; Coudray et al., 2013). Several homologs with speci- et al., 2012). ficity for Zn2+ have been described, including ZitB in E. coli 2. Members of the P-type ATPase family (Figure 1) are present (Chao and Fu, 2004), ZitA in M. tuberculosis (Nies, 2003), in eukaryotes and prokaryotes and, as the name implies, CzcD in B. subtilis (Guffanti et al., 2002)orS. pneumoniae they couple metal transport to the hydrolysis of ATP (Fagan (Kloosterman et al., 2007). and Saier, 1994). Catalytic phosphorylation of the trans- A subclass of CDF exporters,
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