Increased spread and replication efficiency of Listeria monocytogenes in organotypic brain-slices is related to multilocus variable number of tandem repeat analysis (MLVA) complex

BMC Microbiology

Anna Oevermann¹  Torsten Seuberlich¹  Andreas Zurbriggen¹  Joachim Frey³  Michelle Bärtschi¹  Claudia Guldimann² 

[1] Division of Neurological Sciences, Neurocenter, Department of Clinical Research and Veterinary Public Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland;Graduate school for Cellular and Biomedical Sciences, University of Bern, Bern, Switzerland;Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Bern, Bern, Switzerland

关键词: MLVA complex;    Microglia;    Ruminant;    In vitro model;    Plaque test;    Organotypic brain slice;    Neurovirulence;    Rhombencephalitis;    Listeria monocytogenes;   

Others  :  1227629
DOI  :  10.1186/s12866-015-0454-0

 received in 2014-11-10, accepted in 2015-05-28,  发布年份 2015

【 摘 要 】

Background

Listeria (L.) monocytogenes causes fatal infections in many species including ruminants and humans. In ruminants, rhombencephalitis is the most prevalent form of listeriosis. Using multilocus variable number tandem repeat analysis (MLVA) we recently showed that L. monocytogenes isolates from ruminant rhombencephalitis cases are distributed over three genetic complexes (designated A, B and C). However, the majority of rhombencephalitis strains and virtually all those isolated from cattle cluster in MLVA complex A, indicating that strains of this complex may have increased neurotropism and neurovirulence. The aim of this study was to investigate whether ruminant rhombencephalitis strains have an increased ability to propagate in the bovine hippocampal brain-slice model and can be discriminated from strains of other sources. For this study, forty-seven strains were selected and assayed on brain-slice cultures, a bovine macrophage cell line (BoMac) and a human colorectal adenocarcinoma cell line (Caco-2). They were isolated from ruminant rhombencephalitis cases (n = 21) and other sources including the environment, food, human neurolisteriosis cases and ruminant/human non-encephalitic infection cases (n = 26).

Results

All but one L. monocytogenes strain replicated in brain slices, irrespectively of the source of the isolate or MLVA complex. The replication of strains from MLVA complex A was increased in hippocampal brain-slice cultures compared to complex C. Immunofluorescence revealed that microglia are the main target cells for L. monocytogenes and that strains from MLVA complex A caused larger infection foci than strains from MLVA complex C. Additionally, they caused larger plaques in BoMac cells, but not CaCo-2 cells.

Conclusions

Our brain slice model data shows that all L. monocytogenes strains should be considered potentially neurovirulent. Secondly, encephalitis strains cannot be conclusively discriminated from non-encephalitis strains with the bovine organotypic brain slice model. The data indicates that MLVA complex A strains are particularly adept at establishing encephalitis possibly by virtue of their higher resistance to antibacterial defense mechanisms in microglia cells, the main target of L. monocytogenes.

【 授权许可】

   
2015 Guldimann et al.

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【 参考文献 】

• [1]Murray EG. A characterization of listeriosis in man and other animals. Can Med Assoc J. 1955; 72:99-103.
• [2]Low JC, Donachie W. A review of Listeria monocytogenes and listeriosis. Vet J. 1997; 153:9-29.
• [3]Siegman-Igra Y, Levin R, Weinberger M, Golan Y, Schwartz D, Samra Z, Konigsberger H, Yinnon A, Rahav G, Keller N et al.. Listeria monocytogenes infection in Israel and review of cases worldwide. Emerg Infect Dis. 2002; 8:305-310.
• [4]Vital signs: Listeria illnesses, deaths, and outbreaks–United States, 2009–2011. MMWR Morb Mortal Wkly Rep. 2013; 62:448-452.
• [5]The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. Euro Surveill. 2013; 18:20449.
• [6]Sigurdardottir B, Bjornsson OM, Jonsdottir KE, Erlendsdottir H, Gudmundsson S. Acute bacterial meningitis in adults. A 20-year overview. Arch Intern Med. 1997; 157:425-430.
• [7]Mailles A, Lecuit M, Goulet V, Leclercq A, Stahl JP. Listeria monocytogenes encephalitis in France. Med Mal Infect. 2011; 41:594-601.
• [8]Arslan F, Meynet E, Sunbul M, Sipahi OR, Kurtaran B, Kaya S, et al. The clinical features, diagnosis, treatment, and prognosis of neuroinvasive listeriosis: a multinational study. Eur J Clin Microbiol Infect Dis. 2015. doi: 10.1007/s10096-015-2346-5.
• [9]Drevets DA, Bronze MS. Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol Med Microbiol. 2008; 53:151-165.
• [10]Büla CJ, Bille J, Glauser MP. An epidemic of food-borne listeriosis in western Switzerland: description of 57 cases involving adults. Clin Infect Dis. 1995; 20:66-72.
• [11]Oevermann A, Di Palma S, Doherr MG, Abril C, Zurbriggen A, Vandevelde M. Neuropathogenesis of naturally occurring encephalitis caused by Listeria monocytogenes in ruminants. Brain Pathol. 2010; 20:378-390.
• [12]Heim D, Fatzer R, Hornlimann B, Vandevelde M. Frequency of neurologic diseases in cattle. Schweiz Arch Tierheilkd. 1997; 139:354-362.
• [13]Miyashita M, Stierstorfer B, Schmahl W. Neuropathological findings in brains of Bavarian cattle clinically suspected of bovine spongiform encephalopathy. J Vet Med B Infect Dis Vet Public Health. 2004; 51:209-215.
• [14]Oevermann A, Botteron C, Seuberlich T, Nicolier A, Friess M, Doherr MG, Heim D, Hilbe M, Zimmer K, Zurbriggen A et al.. Neuropathological survey of fallen stock: active surveillance reveals high prevalence of encephalitic listeriosis in small ruminants. Vet Microbiol. 2008; 130:320-329.
• [15]Ladds PW, Dennis SM, Cooper RF. Sequential studies of experimentally induced ovine listerial abortion: clinical changes and bacteriologic examinations. Am J Vet Res. 1974; 35:155-160.
• [16]Wilesmith JW, Gitter M. Epidemiology of ovine listeriosis in Great Britain. Vet Rec. 1986; 119:467-470.
• [17]Wagner M, Melzner D, Bago Z, Winter P, Egerbacher M, Schilcher F, Zangana A, Schoder D. Outbreak of clinical listeriosis in sheep: evaluation from possible contamination routes from feed to raw produce and humans. J Vet Med B Infect Dis Vet Public Health. 2005; 52:278-283.
• [18]Killinger AH, Mansfield ME. Epizootiology of listeric infection in sheep. J Am Vet Med Assoc. 1970; 157:1318-1324.
• [19]Dreyer M, Thomann A, Böttcher S, Frey J, Oevermann A. Outbreak investigation identifies a single Listeria monocytogenes strain in sheep with different clinical manifestations, soil and water. Vet Microbiol. 2015. doi: 10.1016/j.vetmic.2015.01.025.
• [20]Cartwright EJ, Jackson KA, Johnson SD, Graves LM, Silk BJ, Mahon BE. Listeriosis outbreaks and associated food vehicles, United States, 1998–2008. Emerg Infect Dis. 2013; 19:1-9.
• [21]Orsi RH, den Bakker HC, Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol. 2011; 301:79-96.
• [22]Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, Brisse S. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 2008; 4:e1000146.
• [23]Sperry KE, Kathariou S, Edwards JS, Wolf LA. Multiple-locus variable-number tandem-repeat analysis as a tool for subtyping Listeria monocytogenes strains. J Clin Microbiol. 2008; 46:1435-1450.
• [24]Liu D. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol. 2006; 55:645-659.
• [25]Brosch R, Chen J, Luchansky JB. Pulsed-field fingerprinting of listeriae: identification of genomic divisions for Listeria monocytogenes and their correlation with serovar. Appl Environ Microbiol. 1994; 60:2584-2592.
• [26]Matloob M, Griffiths M. Ribotyping and automated ribotyping of Listeria monocytogenes. Methods Mol Biol. 2014; 1157:85-93.
• [27]Seeliger HP, Höhne K. Serotyping of Listeria monocytogenes and related species. Methods Microbiol. 1979; 13:31-49.
• [28]Chenal-Francisque V, Lopez J, Cantinelli T, Caro V, Tran C, Leclercq A, Lecuit M, Brisse S. Worldwide distribution of major clones of Listeria monocytogenes. Emerg Infect Dis. 2011; 17:1110-1112.
• [29]McLauchlin J. Distribution of serovars of Listeria monocytogenes isolated from different categories of patients with listeriosis. Eur J Clin Microbiol Infect Dis. 1990; 9:210-213.
• [30]Schuchat A, Swaminathan B, Broome CV. Epidemiology of human listeriosis. Clin Microbiol Rev. 1991; 4:169-183.
• [31]Balandyte L, Brodard I, Frey J, Oevermann A, Abril C. Ruminant rhombencephalitis-associated Listeria monocytogenes alleles linked to a multilocus variable-number tandem-repeat analysis complex. Appl Environ Microbiol. 2011; 77:8325-8335.
• [32]Piffaretti JC, Kressebuch H, Aeschbacher M, Bille J, Bannerman E, Musser JM, Selander RK, Rocourt J. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proc Natl Acad Sci U S A. 1989; 86:3818-3822.
• [33]Wiedmann M, Bruce JL, Keating C, Johnson AE, McDonough PL, Batt CA. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun. 1997; 65:2707-2716.
• [34]Awofisayo A, Amar C, Ruggles R, Elson R, Adak GK, Mook P, Grant KA. Pregnancy-associated listeriosis in England and Wales. Epidemiol Infect. 2015; 143:249-256.
• [35]Swaminathan B, Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect. 2007; 9:1236-1243.
• [36]Datta AR, Laksanalamai P, Solomotis M. Recent developments in molecular sub-typing of Listeria monocytogenes. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2013; 30:1437-1445.
• [37]McLauchlin J, Mitchell RT, Smerdon WJ, Jewell K. Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. Int J Food Microbiol. 2004; 92:15-33.
• [38]Pohl MA, Wiedmann M, Nightingale KK. Associations among Listeria monocytogenes genotypes and distinct clinical manifestations of listeriosis in cattle. Am J Vet Res. 2006; 67:616-626.
• [39]Rocha PR, Lomonaco S, Bottero MT, Dalmasso A, Dondo A, Grattarola C, Zuccon F, Iulini B, Knabel SJ, Capucchio MT et al.. Listeria monocytogenes strains from ruminant rhombencephalitis constitute a genetically homogeneous group related to human outbreak strains. Appl Environ Microbiol. 2013; 79:3059-3066.
• [40]Jeffers GT, Bruce JL, McDonough PL, Scarlett J, Boor KJ, Wiedmann M. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology. 2001; 147:1095-1104.
• [41]Disson O, Lecuit M. Targeting of the central nervous system by Listeria monocytogenes. Virulence. 2012; 3:213-221.
• [42]Guldimann C, Lejeune B, Hofer S, Leib SL, Frey J, Zurbriggen A, Seuberlich T, Oevermann A. Ruminant organotypic brain-slice cultures as a model for the investigation of CNS listeriosis. Int J Exp Pathol. 2012; 93:259-268.
• [43]Sun AN, Camilli A, Portnoy DA. Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect Immun. 1990; 58:3770-3778.
• [44]Roche SM, Velge P, Bottreau E, Durier C, der MN M-v, Pardon P. Assessment of the virulence of Listeria monocytogenes: agreement between a plaque-forming assay with HT-29 cells and infection of immunocompetent mice. Int J Food Microbiol. 2001; 68:33-44.
• [45]Hernandez-Milian A, Payeras-Cifre A. What is new in listeriosis? Biomed Res Int. 2014; 2014:358051.
• [46]Ransohoff RM, Cardona AE. The myeloid cells of the central nervous system parenchyma. Nature. 2010; 468:253-262.
• [47]Rupp S, Aguilar-Bultet L, Jagannathan V, Guldimann C, Drögemüller C, Pfarrer C, et al. A naturally occurring prfA truncation in a Listeria monocytogenes field strain contributes to reduced replication and cell-to-cell spread. Vet Microbiol. 2015. doi: 10.1016/j.vetmic.2015.03.002.
• [48]Bueno VF, Banerjee P, Banada PP, de MA J, Lemes-Marques EG, Bhunia AK. Characterization of Listeria monocytogenes isolates of food and human origins from Brazil using molecular typing procedures and in vitro cell culture assays. Int J Environ Health Res. 2010; 20:43-59.
• [49]Chatterjee SS, Otten S, Hain T, Lingnau A, Carl UD, Wehland J, Domann E, Chakraborty T. Invasiveness is a variable and heterogeneous phenotype in Listeria monocytogenes serotype strains. Int J Med Microbiol. 2006; 296:277-286.
• [50]Van Langendonck N, Bottreau E, Bailly S, Tabouret M, Marly J, Pardon P, Velge P. Tissue culture assays using Caco-2 cell line differentiate virulent from non-virulent Listeria monocytogenes strains. J Appl Microbiol. 1998; 85:337-346.
• [51]Pine L, Kathariou S, Quinn F, George V, Wenger JD, Weaver RE. Cytopathogenic effects in enterocytelike Caco-2 cells differentiate virulent from avirulent Listeria strains. J Clin Microbiol. 1991; 29:990-996.
• [52]Del Corral F, Buchanan RL, Bencivengo MM, Cooke PH. Quantitative comparison of selected virulence-associated characteristics in food and clinical isolates of Listeria. J Food Prot. 1990; 53:1003-1009.
• [53]Roberts AJ, Williams SK, Wiedmann M, Nightingale KK. Some Listeria monocytogenes outbreak strains demonstrate significantly reduced invasion, inlA transcript levels, and swarming motility in vitro. Appl Environ Microbiol. 2009; 75:5647-5658.
• [54]Werbrouck H, Grijspeerdt K, Botteldoorn N, Van PE, Rijpens N, Van DJ, Uyttendaele M, Herman L, Van CE. Differential inlA and inlB expression and interaction with human intestinal and liver cells by Listeria monocytogenes strains of different origins. Appl Environ Microbiol. 2006; 72:3862-3871.
• [55]Cotter PD, Draper LA, Lawton EM, Daly KM, Groeger DS, Casey PG, Ross RP, Hill C. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog. 2008; 4:e1000144.