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Host-Pathogen Adhesion As the Basis of Innovative Diagnostics for Emerging Pathogens

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Host-Pathogen Adhesion As the Basis of Innovative Diagnostics for Emerging Pathogens diagnostics Review Host-Pathogen Adhesion as the Basis of Innovative Diagnostics for Emerging Pathogens Alex van Belkum 1,* , Carina Almeida 2, Benjamin Bardiaux 3 , Sarah V. Barrass 4, Sarah J. Butcher 4, Tu˘gçeÇaykara 5, Sounak Chowdhury 6, Rucha Datar 7, Ian Eastwood 8, Adrian Goldman 4,9, Manisha Goyal 1, Lotta Happonen 6, Nadia Izadi-Pruneyre 3, Theis Jacobsen 3, Pirjo H. Johnson 9, Volkhard A. J. Kempf 10, Andreas Kiessling 9, Juan Leva Bueno 9, Anchal Malik 9, Johan Malmström 6 , Ina Meuskens 11, Paul A. Milner 9, Michael Nilges 3, Nicole Pamme 12 , Sally A. Peyman 9 , Ligia R. Rodrigues 13 , Pablo Rodriguez-Mateos 12, Maria G. Sande 13, Carla Joana Silva 5, Aleksandra Cecylia Stasiak 14 , Thilo Stehle 14, Arno Thibau 10, Diana J. Vaca 10 and Dirk Linke 11,* 1 BioMérieux, Open Innovation & Partnerships, 38390 La Balme Les Grottes, France; [email protected] 2 Biomode, 4715-330 Braga, Portugal; [email protected] 3 Institut Pasteur, Structural Biology and Chemistry, 75724 Paris, France; [email protected] (B.B.); [email protected] (N.I.-P.); [email protected] (T.J.); [email protected] (M.N.) 4 Department of Biological Sciences, University of Helsinki, 00014 Helsinki, Finland; sarah.barrass@helsinki.fi (S.V.B.); sarah.butcher@helsinki.fi (S.J.B.); [email protected] (A.G.) 5 Centre for Nanotechnology and Smart Materials, 4760-034 Vila Nova de Famalicão, Portugal; [email protected] (T.Ç.); [email protected] (C.J.S.) 6 Division of Infection Medicine, Department of Clinical Sciences, Lund University, 22242 Lund, Sweden; Citation: van Belkum, A.; Almeida, [email protected] (S.C.); [email protected] (L.H.); [email protected] (J.M.) C.; Bardiaux, B.; Barrass, S.V.; Butcher, 7 BioMérieux, Microbiology R&D, 38390 La Balme Les Grottes, France; [email protected] S.J.; Çaykara, T.; Chowdhury, S.; 8 Eluceda, Burnley BB11 5UB, UK; [email protected] Datar, R.; Eastwood, I.; Goldman, A.; 9 School of Biomedical Sciences, University of Leeds, Leeds LS2 9JT, UK; [email protected] (P.H.J.); et al. Host-Pathogen Adhesion as the [email protected] (A.K.); [email protected] (J.L.B.); [email protected] (A.M.); Basis of Innovative Diagnostics for [email protected] (P.A.M.); [email protected] (S.A.P.) 10 Emerging Pathogens. Diagnostics Institute for Medical Microbiology and Infection Control, University Hospital, Goethe-University, 2021, 11, 1259. https://doi.org/ 60596 Frankfurt am Main, Germany; [email protected] (V.A.J.K.); [email protected] (A.T.); 10.3390/diagnostics11071259 [email protected] (D.J.V.) 11 Department of Biosciences, University of Oslo, 0316 Oslo, Norway; [email protected] 12 School of Mathematics and Physical Sciences, University of Hull, Hull HU6 7RX, UK; Academic Editors: Xavier [email protected] (N.P.); [email protected] (P.R.-M.) Muñoz-Berbel, Michele Dei and 13 CEB—Centre of Biological Engineering, University of Minho, 4710-057 Braga, Portugal; Miguel A. Pellitero [email protected] (L.R.R.); [email protected] (M.G.S.) 14 Interfaculty Institute of Biochemistry, University of Tübingen, 72076 Tübingen, Germany; Received: 20 April 2021 [email protected] (A.C.S.); [email protected] (T.S.) Accepted: 21 June 2021 * Correspondence: [email protected] (A.v.B.); [email protected] (D.L.) Published: 14 July 2021 Abstract: Infectious diseases are an existential health threat, potentiated by emerging and re-emerging Publisher’s Note: MDPI stays neutral viruses and increasing bacterial antibiotic resistance. Targeted treatment of infectious diseases re- with regard to jurisdictional claims in quires precision diagnostics, especially in cases where broad-range therapeutics such as antibiotics published maps and institutional affil- fail. There is thus an increasing need for new approaches to develop sensitive and specific in vitro iations. diagnostic (IVD) tests. Basic science and translational research are needed to identify key microbial molecules as diagnostic targets, to identify relevant host counterparts, and to use this knowledge in developing or improving IVD. In this regard, an overlooked feature is the capacity of pathogens to adhere specifically to host cells and tissues. The molecular entities relevant for pathogen–surface Copyright: © 2021 by the authors. interaction are the so-called adhesins. Adhesins vary from protein compounds to (poly-)saccharides Licensee MDPI, Basel, Switzerland. or lipid structures that interact with eukaryotic host cell matrix molecules and receptors. Such interac- This article is an open access article tions co-define the specificity and sensitivity of a diagnostic test. Currently, adhesin-receptor binding distributed under the terms and is typically used in the pre-analytical phase of IVD tests, focusing on pathogen enrichment. Further conditions of the Creative Commons exploration of adhesin–ligand interaction, supported by present high-throughput “omics” technolo- Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ gies, might stimulate a new generation of broadly applicable pathogen detection and characterization 4.0/). tools. This review describes recent results of novel structure-defining technologies allowing for Diagnostics 2021, 11, 1259. https://doi.org/10.3390/diagnostics11071259 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, 1259 2 of 22 detailed molecular analysis of adhesins, their receptors and complexes. Since the host ligands evolve slowly, the corresponding adhesin interaction is under selective pressure to maintain a constant receptor binding domain. IVD should exploit such conserved binding sites and, in particular, use the human ligand to enrich the pathogen. We provide an inventory of methods based on adhesion factors and pathogen attachment mechanisms, which can also be of relevance to currently emerging pathogens, including SARS-CoV-2, the causative agent of COVID-19. Keywords: adhesin; receptor; infectious diseases; diagnostics 1. Introduction Infectious diseases, particularly those caused by potentially lethal viruses and antibiotic- resistant bacteria, were one of the key issues on the agenda of the G7-Summit in Germany in 2015 (https://www.g7uk.org/new-international-approach-to-combat-emerging-health- threats-as-crucial-g7-health-talks-begin/, accessed on 21 June 2021) (see Table1 for a review of the currently most relevant antibiotic resistant microorganisms). After the summit, every major health authority, including the World Health Organization (WHO), confirmed that the (re-)emergence of infectious diseases in general and the decreasing efficacy of antimicrobials are major medical concerns, as antimicrobial therapies are starting to fail (Table1) and deadly viruses cause serious global outbreaks [1]. Moreover, it is estimated that around 30% of bacteria responsible for hospital associated infections are antibiotic resistant, with the number of infections being about nine million each year in Europe alone [2]. Clinical misdiagnosis can lead to antibiotic resistance when proper diagnostic methods are not used and patients are prescribed unnecessary treatments [3]. Thus, novel diagnostic tests are urgently needed to prevent (re-)emerging infections and to better treat infections by clinically relevant antibiotic resistant pathogens. Therefore, continued academic and industrial investment in new in vitro diagnostic (IVD) tests is urgently required to tackle antimicrobial resistance (AMR), (multi)drug-resistance (MDR) or even pan-resistance (PDR) [4–6]. Clearly, prior to infection, pathogens colonize their host organisms via adhesion: the binding of microbial molecules—adhesins—to specific host counterparts. Consequently, adhesins can be used to specifically enrich pathogens. Below, we explore this concept from a variety of viewpoints. Table 1. WHO priority bacterial pathogens and their clinically relevant antibiotic resistance phe- notypes which render treatment problems (adapted from www.who.int (accessed on 21 June 2021) and [7]). ESBL: extended spectrum beta-lactamase. Priority 1: Critical Acinetobacter baumannii carbapenem-resistant Pseudomonas aeruginosa carbapenem-resistant Enterobacteriales carbapenem-resistant, ESBL-producing Priority 2: High Enterococcus faecium vancomycin-resistant Staphylococcus aureus methicillin-resistant, vancomycin-intermediate and resistant Helicobacter pylori clarithromycin-resistant Campylobacter spp. fluoroquinolone-resistant Salmonellae fluoroquinolone-resistant Neisseria gonorrhoeae cephalosporin-resistant, fluoroquinolone-resistant Priority 3: Medium Streptococcus pneumoniae penicillin-non-susceptible Haemophilus influenzae ampicillin-resistant Shigella spp. fluoroquinolone-resistant Diagnostics 2021, 11, 1259 3 of 22 Diagnostics 2021, 11, x FOR PEER REVIEW 3 of 23 1.1. Microbial Adhesion, Colonization and Host Infection The severity of an infectious disease depends on the level of invasiveness and the extent1.1. Microbial of host Adhesion, cell and tissue Colonization damage and caused Host Infection by the pathogen involved [8]. A varying degree of virulenceThe severity can be of observedan infectious across disease different depends pathogens on the level and of among invasiveness different and strains the of a singleextent pathogenof host cell [ 9and]. Virulence tissue damage is a complicated caused by the concept pathogen in involved microbial [8]. pathogenesis A varying de- since it dependsgree of virulence not only can on thebe observed infectious
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