Mitogen-activated protein kinases are required for effective infection of human choroid plexus epithelial cells by Listeria monocytogenes

Dinner, Stefanie; Kaltschmidt, Julian; Stump-Guthier, Carolin; Hetjens, Svetlana; Ishikawa, Hiroshi; Tenenbaum, Tobias; Schroten, Horst; Schwerk, Christian

doi:10.1016/j.micinf.2016.09.003

Cited by 29 publications

(30 citation statements)

References 53 publications

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“…It is noteworthy that this effect could be demonstrated despite the apically about 10-fold amount of exposed surface area, since the filter only allows limited accessibility to the basolateral cell side, where the pores are the only possible point of contact. This corresponds to previous findings concerning polar invasion of other bacteria such as N. meningitidis, S. suis and L. monocytogenes (Borkowski et al 2014;Dinner et al 2016;Dinner et al 2017;Grundler et al 2013;Schwerk et al 2012). It calls, however, the previous assumption into question that the occasionally observed choroid plexitis is caused secondarily after CSF infection via the BBB.…”

Section: Discussionsupporting

confidence: 89%

Virulence factor-dependent basolateral invasion of choroid plexus epithelial cells by pathogenic Escherichia coli in vitro

Rose

Häuser

Stump-Guthier

et al. 2018

FEMS Microbiology Letters

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Escherichia coli is the most common Gram-negative causative agent of neonatal meningitis and E. coli meningitis is associated with high morbidity and mortality. Previous research has been carried out with regard to the blood–brain barrier and thereby unveiled an assortment of virulence factors involved in E. coli meningitis. Little, however, is known about the role of the blood–cerebrospinal fluid (CSF) barrier (BCSFB), in spite of several studies suggesting that the choroid plexus (CP) is a possible entry point for E. coli into the CSF spaces. Here, we used a human CP papilloma (HIBCPP) cell line that was previously established as valid model for the study of the BCSFB. We show that E. coli invades HIBCPP cells in a polar fashion preferentially from the physiologically relevant basolateral side. Moreover, we demonstrate that deletion of outer membrane protein A, ibeA or neuDB genes results in decreased cell infection, while absence of fimH enhances invasion, although causing reduced adhesion to the apical side of HIBCPP cells. Our findings suggest that the BCSFB might constitute an entry point for E. coli into the central nervous system, and HIBCPP cells are a valuable tool for investigating E. coli entry of the BCSFB.

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Section: Discussionsupporting

confidence: 89%

Virulence factor-dependent basolateral invasion of choroid plexus epithelial cells by pathogenic Escherichia coli in vitro

Rose

Häuser

Stump-Guthier

et al. 2018

FEMS Microbiology Letters

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“…Activation of MAPKs Erk1/2 and p38 signaling preferentially from the basolateral side of the CP epithelium has been described in an in vitro model of the B-CSF barrier based on human CP papilloma cells following exposure to Listeria monocytogenes. Concurrent inhibition of MAPK signaling pathways potentially reduces infection [142]. Streptococus suis (S. suis) can cross the B-CSF barrier within endocytic vacuoles and there is some evidence supporting a "Trojan horse" mechanism using polymorphonuclear leukocytes.…”

Section: Bacterial Infectionsmentioning

confidence: 99%

Choroid plexus and the blood–cerebrospinal fluid barrier in disease

Solar

Zamani

Kubíčková

et al. 2020

Fluids Barriers CNS

174

142

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The choroid plexus (CP) forming the blood-cerebrospinal fluid (B-CSF) barrier is among the least studied structures of the central nervous system (CNS) despite its clinical importance. The CP is an epithelio-endothelial convolute comprising a highly vascularized stroma with fenestrated capillaries and a continuous lining of epithelial cells joined by apical tight junctions (TJs) that are crucial in forming the B-CSF barrier. Integrity of the CP is critical for maintaining brain homeostasis and B-CSF barrier permeability. Recent experimental and clinical research has uncovered the significance of the CP in the pathophysiology of various diseases affecting the CNS. The CP is involved in penetration of various pathogens into the CNS, as well as the development of neurodegenerative (e.g., Alzheimer´s disease) and autoimmune diseases (e.g., multiple sclerosis). Moreover, the CP was shown to be important for restoring brain homeostasis following stroke and trauma. In addition, new diagnostic methods and treatment of CP papilloma and carcinoma have recently been developed. This review describes and summarizes the current state of knowledge with regard to the roles of the CP and B-CSF barrier in the pathophysiology of various types of CNS diseases and sets up the foundation for further avenues of research. Publisher's NoteSpringer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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“…Human choroid plexus papilloma (HIBCPP) cells [ 40 ] were cultivated on cell culture inserts and were maintained in DMEM/HAM’s F12 1:1 supplemented with 10 or 1% inactivated fetal calf serum (FCS), 4 mM L-Glutamine, streptomycin (100 μg/ml) and penicillin (100 U/ml), insulin (5 μg/ml), previously described by Dinner et al [ 41 ]. For control experiments, the human rhabdomyosarcoma (RD) cell line was used, which is commonly used to propagate NPEV.…”

Section: Methodsmentioning

confidence: 99%

“…For the purpose of a filter-based experimental set-up, HIBCPP cells were seeded on inverted culture filter inserts (Millipore and Sarsted, Germany; pore diameter 5.0 μm, pore density 6.0 × 10 5 pores/cm 2 , area 0.33 cm 2 ). The inverted cell culture system was chosen to allow physiologically relevant infection from the basolateral cell side [ 41 , 42 ]. Evaluation of barrier integrity over the course of the experiment was performed through measurement of transepithelial electrical resistance (TEER) using a tissue voltohmmeter (Millipore, Germany) and permeability analysis of dextran-TexasRed (Invitrogen, Germany) tracer solution (100 μg/ml) following the pre-described methodology [ 19 , 39 ].…”

Section: Methodsmentioning

confidence: 99%

Strain-dependent effects of clinical echovirus 30 outbreak isolates at the blood-CSF barrier

Dahm

Adams

Boettcher

et al. 2018

J Neuroinflammation

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BackgroundEchovirus (E) 30 (E-30) meningitis is characterized by neuroinflammation involving immune cell pleocytosis at the protective barriers of the central nervous system (CNS). In this context, infection of the blood-cerebrospinal fluid barrier (BCSFB), which has been demonstrated to be involved in enteroviral CNS pathogenesis, may affect the tight junction (TJ) and adherens junction (AJ) function and morphology.MethodsWe used an in vitro human choroid plexus epithelial (HIBCPP) cell model to investigate the effect of three clinical outbreak strains (13-311, 13-759, and 14-397) isolated in Germany in 2013, and compared them to E-30 Bastianni. Conducting transepithelial electrical resistance (TEER), paracellular dextran flux measurement, quantitative real-time polymerase chain reaction (qPCR), western blot, and immunofluorescence analysis, we investigated TJ and AJ function and morphology as well as strain-specific E-30 infection patterns. Additionally, transmission electron and focused ion beam microscopy electron microscopy (FIB-SEM) was used to evaluate the mode of leukocyte transmigration. Genome sequencing and phylogenetic analyses were performed to discriminate potential genetic differences among the outbreak strains.ResultsWe observed a significant strain-dependent decrease in TEER with strains E-30 Bastianni and 13-311, whereas paracellular dextran flux was only affected by E-30 Bastianni. Despite strong similarities among the outbreak strains in replication characteristics and particle distribution, strain 13-311 was the only outbreak isolate revealing comparable disruptive effects on TJ (Zonula Occludens (ZO) 1 and occludin) and AJ (E-cadherin) morphology to E-30 Bastianni. Notwithstanding significant junctional alterations upon E-30 infection, we observed both para- and transcellular leukocyte migration across HIBCPP cells. Complete genome sequencing revealed differences between the strains analyzed, but no explicit correlation with the observed strain-dependent effects on HIBCPP cells was possible.ConclusionThe findings revealed distinct E-30 strain-specific effects on barrier integrity and junctional morphology. Despite E-30-induced barrier alterations leukocyte trafficking did not exclusively occur via the paracellular route.Electronic supplementary materialThe online version of this article (10.1186/s12974-018-1061-4) contains supplementary material, which is available to authorized users.

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Mitogen-activated protein kinases are required for effective infection of human choroid plexus epithelial cells by Listeria monocytogenes

Cited by 29 publications

References 53 publications

Virulence factor-dependent basolateral invasion of choroid plexus epithelial cells by pathogenic Escherichia coli in vitro

Virulence factor-dependent basolateral invasion of choroid plexus epithelial cells by pathogenic Escherichia coli in vitro

Choroid plexus and the blood–cerebrospinal fluid barrier in disease

Strain-dependent effects of clinical echovirus 30 outbreak isolates at the blood-CSF barrier

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