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Listeria Monocytogenes: a Paradigm Among Intracellular Bacterial Pathogens Javier Pizarro-Cerdá, Pascale Cossart

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Listeria Monocytogenes: a Paradigm Among Intracellular Bacterial Pathogens Javier Pizarro-Cerdá, Pascale Cossart Microbe Profile: Listeria monocytogenes: a paradigm among intracellular bacterial pathogens Javier Pizarro-Cerdá, Pascale Cossart To cite this version: Javier Pizarro-Cerdá, Pascale Cossart. Microbe Profile: Listeria monocytogenes: a paradigm among intracellular bacterial pathogens. Open Microbiology Journal, Bentham Open, 2019. hal-02734952 HAL Id: hal-02734952 https://hal.archives-ouvertes.fr/hal-02734952 Submitted on 2 Jun 2020 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. 1 Listeria monocytogenes: a paradigm among intracellular bacterial pathogens 2 3 Javier Pizarro-Cerdá1 and Pascale Cossart2 4 1Yersinia Research Unit, Department of Microbiology and 2Department of Cell Biology & Infection, 5 Institut Pasteur - 75015 Paris, FRANCE 6 7 8 9 Figure. The cell infectious process 10 L. monocytogenes induces its entry into non-phagocytic cells via the activity of bacterial 11 surface and secreted effectors that promote remodeling of the plasma membrane and 12 bacterial engulfment. Secreted molecules allow vacuolar disruption and bacterial 13 translocation to the host cell cytoplasm, where host metabolites are catabolized and the 14 actin cytoskeleton is hijacked to favor cell-to-cell spread. For survival, L. monocytogenes 15 manipulates organelles such as mitochondria and lysosomes, as well as host gene 16 expression. Major bacterial effectors are mentioned for each intracellular step (from 17 Pizarro-Cerdá J, & Cossart P. 2018. Listeria monocytogenes: cell biology of invasion and 18 intracellular growth. Microbiology Spectrum 6: GPP3-0013-2018.s). 19 20 21 22 Abstract 23 Listeria monocytogenes is a food-borne bacterial pathogen responsible for listeriosis, a 24 disease characterized by occasional febrile gastroenteritis in immunocompetent 25 individuals, abortions in pregnant women, meningitis in the newborn, and fatal bacteremia 26 in immunocompromised individuals or the elderly. L. monocytogenes capacity to produce 27 disease is intimately associated with its potential to traverse several human barriers 28 (including the intestinal, the placental and the blood/brain barriers), to promote its 29 internalization within diverse populations of epithelial cells, and to proliferate in the intra- 30 cytoplasmic environment while escaping host immune responses. L. monocytogenes is 31 often regarded as a paradigm for intracellular parasitism. 32 33 Taxonomy 34 Domain Bacteria, phylum Firmicutes, class Bacilli, order Bacillales, family Listeriaceae, 35 genus Listeria, species L. monocytogenes. 36 37 Properties 38 L. monocytogenes are Gram-positive bacilli, non-spore forming, facultatively anaerobic, 39 catalase-positive, rod-shaped circa 0.5 µm x 2-3 µm. At 20-25°C L. monocytogenes 40 behaves as a flagellated environmental saprophyte; at 37°C flagellar expression is 41 repressed and L. monocytogenes activates a genetic program that allows bacterial life as 42 a facultative intracellular pathogen. 43 44 Genome 45 L. monocytogenes EGDe was the first strain to be sequenced (Glaser et al. 2001), with a 46 genome of 2,944,528 base pairs, an average G+C content of 38%, 2853 protein coding 47 sequences, and 89.2% of coding regions. No plasmids are present in L. monocytogenes 48 EGDe and 1 to 3 prophage regions have been described in different sequenced strains. 6 49 rRNA operons (16S-23S-5S) and 67 tRNA genes have been reported. The Listeria 50 Pathogenicity Island-I (LIPI-I) encodes key factors required for bacterial growth and 51 survival, while the inlA-inlB locus codes for surface proteins driving bacterial cell 52 internalization. 53 54 Phylogeny & Genomic Population Structure 55 Four major evolutionary phylogenetic lineages (lineages I, II, III and IV) have been 56 described for the species L. monocytogenes, comprising 13 different serotypes: 1/2b, 3b, 57 4b, 4d, 4e and 7 (lineage I), 1/2a, 3a, 3c and 1/2c (lineage II), 4a, 4c and 4b (lineages III 58 and IV). Traditionally, serotype 4b (lineage I) has been associated most frequently with 59 human listeriosis cases. Using a multi-locus sequence typing scheme based on the 60 sequence analysis of seven housekeeping genes, different clonal complexes (CCs) have 61 been identified within each evolutionary lineage: CC1, CC2, CC4 and CC6 (serotype 4b, 62 lineage I) are significantly associated to human clinical isolates, while CC121 and CC9 63 (serotypes 1/2a and 1/2c respectively, lineage II) are associated to food isolates (Maury et 64 al., 2016). 65 66 Key Features & Discoveries 67 L. monocytogenes was first identified in 1926 in England by E.G.D. Murray as a pathogen 68 causing a large mononuclear leucocytosis in rabbits. Soon afterwards, in 1927, L. 69 monocytogenes was described by J.H.H. Pirie as a pathogen causing liver and spleen 70 necrosis in gerbils in South Africa. In 1962, G.B. Mackaness used for the first time L. 71 monocytogenes as a model to understand immune responses against intracellular 72 pathogens, discovering that recovery from primary infection and protection against a 73 secondary infection are cell-mediated, antibodies playing no role in these processes. In 74 1983, L. monocytogenes was identified as responsible for human food-borne infections 75 after a major listeriosis outbreak in Canada, originating from contaminated coleslaw. In 76 1989, L.G. Tilney and D.A. Portnoy described the intracellular lifestyle of L. 77 monocytogenes, revealing that after bacterial internalization and release in the host cell 78 cytoplasm, the bacteria polymerize actin structures that trigger intracellular motility and 79 cell-to-cell spread (Tilney and Portnoy, 1989). In the 1990s, the P. Cossart team identified 80 internalins InlA and InlB as bacterial surface molecules required for L. monocytogenes 81 host cell invasion. Interactions between InlA and InlB with their cellular receptors E- 82 cadherin and c-Met respectively are species-specific, and are both required for human 83 placental infection. In contrast, a transgenic mouse model expressing human E-cadherin 84 allowed to demonstrate that only the InlA/E-cadherin interaction is required for intestinal 85 barrier translocation through goblet cells (Lecuit et al., 2001). Upon internalization in goblet 86 cells, L. monocytogenes resides in a vacuole and transcytosis leads to bacterial 87 translocation to the lamina propria. In other cells, the combined activity of the pore-forming 88 toxin Listeriolysin O (LLO), the metalloprotease Mpl, the phospholipases PlcA and PlcB as 89 well as the pheromone pPplA, favor disruption of the vacuole. Cytosolic L. monocytogenes 90 imports host metabolites via the phosphate transporter Hpt and the lipate protein ligase 91 LplA, and the bacterial surface protein ActA promotes actin-based cytoplasmic movement 92 and cell-to-cell spread. The secreted effectors InlC, OfrX and LntA influence host gene 93 expression, while extracellular LLO mediates entry and remodeling of mitochondria and 94 lysosomes during the infectious process. A subset of L. monocytogenes strains from 95 lineage I frequently associated to human listeriosis outbreaks encode a bacteriocin called 96 Listeriolysin S that modulates the host intestinal microbiota thereby favoring intestinal 97 infection. An attenuated L. monocytogenes strain has been recently proposed as a vector 98 for cancer immunotherapy. Taken together, L. monocytogenes is currently one of the best 99 studied intracellular pathogens (Radoshevich and Cossart, 2018). 100 101 Open Questions 102 • Which mechanisms trigger L. monocytogenes tropism and traversal of the central 103 nervous system? 104 • Which bacterial species are specifically targeted by Listeriolysin S in the human intestinal 105 tract? 106 • Are there additional bacterial factors responsible for the increased virulence associated 107 to lineage I L. monocytogenes strains? 108 • Is there a special niche in the environment for Listeria species? 109 110 References 111 112 Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, Berche P, Bloecker H, 113 Brandt P, Chakraborty T, Charbit A, Chetouani F, Couvé E, de Daruvar A, Dehoux P, 114 Domann E, Domínguez-Bernal G, Duchaud E, Durant L, Dussurget O, Entian KD, Fsihi H, 115 García-del Portillo F, Garrido P, Gautier L, Goebel W, Gómez-López N, Hain T, Hauf J, 116 Jackson D, Jones LM, Kaerst U, Kreft J, Kuhn M, Kunst F, Kurapkat G, Madueno E, 117 Maitournam A, Vicente JM, Ng E, Nedjari H, Nordsiek G, Novella S, de Pablos B, Pérez-Diaz 118 JC, Purcell R, Remmel B, Rose M, Schlueter T, Simoes N, Tierrez A, Vázquez-Boland JA, 119 Voss H, Wehland J, & Cossart P. (2001). Comparative genomics of Listeria species. Science 120 294, 849-52. 121 122 Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C, Babinet C, 123 Cossart P. (2001). A transgenic model for listeriosis: role of internalin in crossing the intestinal 124 barrier. Science 292, 1722-1725. 125 126 Maury MM, Tsai YH, Charlier C, Touchon M, Chenal-Francisque V, Leclercq A, Criscuolo A, 127 Gaultier C, Roussel S, Brisabois A, Disson O, Rocha EPC, Brisse S, Lecuit M. (2016). 128 Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet. 48, 129 308-313. 130 131 Radoshevich L, & Cossart P. (2018). Listeria monocytogenes: towards a complete picture of its 132 physiology and its virulence. Nat Rev Microbiol. 16, 32-46. 133 134 Tilney LG & Portnoy DA. (1989). Actin filaments and the growth, movement and spread of the 135 intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 109, 1597-608. 136 137 138 139 140 We declare no conflict of interest. .
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