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Meningococci were also isolated from the CSF. Due to the absence of bacteremia, it was suggested that N. In rhesus macaques, commensal neisseria bacteria RM Neisseria were shown to be transmitted between animals and naturally colonized the epithelium covering the cribriform plate , suggesting that migration of neisseria bacteria along the olfactory pathway is not a phenomenon that is observed only in animals experimentally inoculated with pathogenic N.

It has been hypothesized that these harsh environmental conditions may irritate the mucus membranes such as the olfactory mucosa and enable N.

These data suggest that N. The mechanisms by which N. The meninges and the subarachnoid space extend over the cribriform plate and further into the olfactory foramen, where the olfactory nerves pass through the cribriform plate , Bacteria traveling along the olfactory pathway may potentially invade the meninges after traversing the cribriform plate, and subsequently enter the CSF.

However, there is a positive pressure from the brain to the nasal lymphatics due to the drainage of CSF through the cribriform plate, and it is unknown how N.

The olfactory pathway has been identified as a route of CNS invasion by B. It was also shown that when colonization occurred in only one side of the nasal cavity, wild-type B.

Combined, these data suggest that B. However, it might be the case that an absence of capsule does diminish translocation via the olfactory or trigeminal nerves, since it is not possible to definitively compare with the presence of capsule, due to hematogenous spread in the latter case.

It may be noted that mice, like most mammals, are naturally susceptible to melioidosis. The mechanisms by which B. This neuronal loss led to the degeneration of olfactory axons within 24 to 48 h, and the axon-devoid, hollow olfactory nerve fascicles, surrounded by olfactory ensheathing cells, provided an open conduit for bacterial passage from the nasal cavity through the cribriform plate and into the nerve fiber layer of the olfactory bulb.

By migrating within the nerve sheath, B. This may also explain why B. During our initial studies in mice, we also demonstrated that B.

We have now confirmed that B. Although there is currently no direct evidence of B. Our unpublished data also demonstrate that following the inhalation of aerosolized B.

Second, for human cases of primary neurological melioidosis, Currie et al. In addition to our animal studies, these data provide evidence that B.

Furthermore, the trigeminal route of CNS invasion may explain the brain stem-related neurological presentations of melioidosis patients, without requiring frank encephalitis.

In ruminants naturally infected with L. Similar findings are observed in human cases of L. Of the cranial nerves, the trigeminal nerve pathway is thought to represent a primary route by which L.

It has been proposed that L. However, binding of L. In animals spontaneously infected and experimentally infected with L.

In a mouse model of brain stem encephalitis, L. Following this, bacteria were then observed within the brain stem but not in other regions of the brain.

In vivo and in vitro studies have demonstrated that colony-stimulating factor 1-dependent cells including macrophages and dendritic cells facilitate the neuronal spread of L.

Following replication and escape from the phagosome in colony-stimulating factor 1-dependent cells, L. Indeed, the presence of L.

In vivo , herpesviruses demonstrate a tropism for the olfactory epithelium but not the respiratory epithelium , — Expression of the herpesvirus receptors heparan sulfate and nectin-1 on the apical side of the olfactory epithelium may facilitate binding to the neuroepithelium , In the respiratory epithelium, these receptors are either expressed on the basal side of the epithelium and are thus inaccessible or not highly expressed , Herpes simplex virus type 1 , bovine herpesvirus 5 , and equine herpesvirus 9 , spread from the nasal mucosa to the CNS via the olfactory nerves in animal models of infection.

In bovine herpesvirus 5 CNS invasion, the viral protein Us9 and the glycine-rich epitope region of glycoprotein E are required for transport from the olfactory sensory neurons to the olfactory bulb , In suckling hamsters, equine herpesvirus 9 antigen was detected within olfactory sensory neurons 12 h after intranasal infection At 48 h postinfection, viral antigen was detected within the olfactory nerve and olfactory bulb, and at 60 h postinfection, virus was observed within the frontal and temporal lobes of the cerebral cortex.

Some positive staining occurred within the trigeminal nerve, the trigeminal ganglia, and the region where the trigeminal sensory nerve root connects to the brain stem, although this was observed at the later time points, suggesting that the olfactory nerve is likely to be the primary route of infection Interestingly, Shivkumar et al.

In this model, the virus rarely reached the olfactory bulbs within the brain. However, in another study, herpes simplex virus type 1 was isolated from the olfactory bulbs and higher brain regions of mice 3 days after intranasal inoculation In a study of human autopsy material, Harberts et al.

In the same study, the prevalence of herpesvirus 6 within the nasal mucosa was determined in 3 cohorts of patients: Overall, herpesvirus 6 DNA was detected in These findings suggest that the nasal cavity may be a reservoir for herpesvirus 6 and that virus within the nasal cavity may travel to the olfactory bulbs and tract via the olfactory pathway Immunohistological evidence from fatal cases of herpes simplex encephalitis demonstrated that herpes simplex virus type 1 antigen was detected within the olfactory tract, the olfactory cortex, and regions of the limbic system that are connected by the olfactory pathway.

In contrast, viral antigen was not detected within the trigeminal pathway Combined, these studies suggest that the olfactory route of CNS entry is highly relevant in human cases of symptomatic and asymptomatic herpesvirus infections.

The role of the trigeminal nerve as a portal of entry for herpesviruses in humans is less clear, although the sensory neurons of the trigeminal ganglia are the principal site of herpes simplex virus type 1 latent infection in humans , In ferrets intranasally infected with different H5N1 strains, three-dimensional 3D imaging demonstrated that brain lesions were distributed i along the olfactory pathway, ii along the olfactory pathway and within the brain stem, or iii surrounding the brain vasculature These data suggest that there may be different routes of entry used by H5N1 strains; however, the olfactory pathway was identified as the most common route used by the small number of strains that were investigated The neurovirulence of influenza A virus subtypes may be influenced by the ability of the virus to disseminate from the olfactory bulb into other regions of the brain , which in turn may be controlled by the host immune response.

The infection was therefore restricted to the neuroepithelium and did not spread to the olfactory bulb. This suggested that apoptosis of olfactory sensory neurons might be a mechanism by which the host is protected from microbial invasion from the nasal cavity Influenza A virus also stimulates a host proinflammatory cytokine response within the olfactory bulb , which may also act to protect the host from further CNS invasion Autopsy of a severely immunocompromised month-old infant revealed influenza A virus antigen within the olfactory bulb, olfactory tract, and gyrus rectus, which is located inferolaterally to the olfactory bulb Viral antigen was not detected within any other regions of the CNS, the respiratory tract, or any other organs.

Viral RNA was also not detected within plasma, suggesting that viremia was not present. These findings provide evidence for influenza A virus entry into the CNS via the olfactory route in a severely immunocompromised infant Paramyxoviruses, including Nipah virus, Hendra virus, and parainfluenza virus, may enter the CNS directly from the nasal mucosa.

In vivo , the Sendai strain of parainfluenza virus infected mouse olfactory sensory neurons, but not sustentacular cells, and traveled to the glomeruli of the olfactory bulb , Infection of second-order neurons and virus spread to the rest of the brain did not occur , — The Sendai virus nucleoprotein gene was consistently detected within the olfactory bulb for up to days postinfection, indicating that persistence may occur within the olfactory bulb In hamsters, Nipah virus was detected in olfactory sensory neurons as they passed through the cribriform plate into the olfactory bulb, providing evidence of direct brain infection following intranasal infection Similar results were reported for a porcine model of Nipah virus infection, in which Nipah virus antigen was detected within a cross section of the olfactory nerve Temporal analysis demonstrated that Nipah virus entered the olfactory bulb within 4 days in mice , whereas the virus spread from the olfactory nerve to the granular cells of the olfactory bulb within 7 days in pigs The related Hendra virus was also shown to target the olfactory pathway and to invade the brain directly from the nasal cavity in the absence of viremia in a mouse model of encephalitis Thus, it is likely that Nipah virus exploits both the hematogenous and olfactory routes of invasion.

Eastern, western, and Venezuelan equine encephalitis viruses can cause encephalitis in horses and humans and are transmitted by mosquitoes or following aerosol exposure.

Using a bioluminescent western equine encephalitis virus, Phillips et al. The bioluminescent signal was initially detected in the nasal turbinates and olfactory bulb and was amplified in the basal nuclei, thalamus, and hypothalamus.

The distribution of lesions within the brain and the detection of viral antigen by immunohistochemistry supported the olfactory pathway as the route of infection and suggested that the trigeminal nerve may provide a secondary conduit to the brain Venezuelan equine encephalitis virus also targeted both the olfactory primary route and trigeminal secondary route nerve pathways for CNS entry , whereas eastern equine encephalitis virus appeared to infect only the olfactory nerve In CD-1 mice, ablation of the olfactory epithelium and the main olfactory bulb prevented invasion of Venezuelan equine encephalitis virus into the brain via the olfactory nerve; however, the virus was still able to spread to the CNS along the trigeminal nerve Interestingly, replication of Venezuelan equine encephalitis virus within the nasal mucosa induced the expression of proinflammatory cytokines, matrix metalloproteinase-9, and intracellular adhesion molecule 1 within the olfactory bulb, which led to subsequent breakdown of the BBB These events enabled circulating virus to penetrate the brain, suggesting that in addition to the olfactory and trigeminal routes of entry, Venezuelan equine encephalitis virus may also enter the CNS by a hematogenous route.

Among the members of the Rhabdoviridae family, rabies virus and vesicular stomatitis virus within the nasal cavity directly invade the olfactory bulbs within the brain.

In a fatal human case of airborne rabies encephalitis, rabies virions were observed only within the nerve fibers of the olfactory bulb, not in any other regions of the brain Data from animal studies have also demonstrated that intranasally delivered rabies virus selectively targets the olfactory epithelium and migrates to the olfactory bulb, including the glomeruli, mitral cells, and tufted cells Rabies virus antigen was also detected in the mouse trigeminal nerve.

The tropism of rabies virus to the olfactory epithelium may be due to the expression by olfactory sensory neurons of neural cell adhesion molecule , which was identified as a receptor for rabies virus in vitro Similar to rabies virus, intranasal vesicular stomatitis virus infected the olfactory epithelium, but not the respiratory epithelium, in a mouse model By 6 h postinfection, viral antigen was observed within the olfactory sensory neurons.

In contrast to the case with rabies virus, the trigeminal nerve was not implicated as a portal of CNS entry for vesicular stomatitis virus Naegleria fowleri is a free-living amoeba that causes primary amoebic meningoencephalitis, a rare but almost always fatal disease in humans.

Contaminated tap water used to reconstitute saline for nasal irrigation or for ablution of the nasal cavity has also been implicated as a source of infection , Pathological investigations of fatal human cases revealed hemolytic, necrotic encephalitis of the olfactory area, the contiguous forebrain, and the cerebellum , The suspected route of CNS entry was the olfactory route, due to the presence of amoebae and acute inflammation within the nasal mucosa and the olfactory nerve bundles , In murine models of the early stages of primary amoebic meningoencephalitis, intranasal N.

In vivo studies have shown that N. Despite this host response, by 12 h, N. In vitro , it was shown that both live trophozoites and crude total N. A kDa cysteine protease of N.

Penetration of the olfactory epithelium in mice occurred without cellular disruption or damage , and microscopy studies have shown that N.

A recent study demonstrated that N. Balamuthia mandrillaris , an opportunistic free-living amoeba that can cause granulomatous amoebic encephalitis, was also shown to enter the CNS directly from the nasal cavity after penetrating the olfactory epithelium and cribriform plate in immunodeficient mice following intranasal infection However, the implications of these findings in humans are unclear, as B.

The encapsulated yeast Cryptococcus neoformans is an important cause of fungal meningoencephalitis worldwide and can enter the CNS by penetrating the BBB by use of transcellular, paracellular, and Trojan horse mechanisms following blood-borne dissemination from the lungs as reviewed elsewhere [ ].

Although the hematogenous route of CNS entry is well accepted for cryptococcal meningoencephalitis, some strains of C. These findings prompted investigations into the possibility of an alternative direct route of CNS entry from the nose.

No cryptococci were located within the lamina propria or the olfactory epithelium, and thus the authors suggested that C.

Using a guinea pig model, Lima and Vital provided further evidence that the olfactory route is unlikely to represent a portal of C. In contrast, the fungal infection rhinocerebral mucormycosis has been demonstrated to spread to the brain via the trigeminal nerve.

Rhinocerebral mucormycosis refers to infections caused by fungi within the order Mucorales and usually affects individuals with poorly controlled diabetes mellitus or the immunocompromised.

These organisms display a predilection for the nasal cavity and paranasal sinuses; from these sites, the organisms typically invade blood vessel walls and then spread to the cavernous sinus, internal carotid artery, and brain , — However, fungal hyphae and lesions have been demonstrated within the trigeminal nerve and the pons within the brain stem in the absence of leptomeningitis, suggesting that direct invasion occurred from the sinuses to the brain along the trigeminal nerve , The perineural route of CNS entry was thought to be atypical; however, a study of the histologic features of patients with mucormycosis demonstrated that perineural invasion, characterized by fungal hyphae within the perineurium that surrounds the nerves, was a common feature that occurred concurrently with angioinvasion The mechanisms of rhinocerebral mucormycosis CNS infection have not been investigated.

A wide range of microbes can invade the CNS, and any organisms that can enter the CSF have the potential to cause meningitis. These nerves are well recognized as portals of entry for many viruses, as well as protozoa and fungi, and there is now evidence from animal models that some bacteria can infect the brain via the olfactory and trigeminal nerves.

The purpose of this review is to highlight these alternative routes of entry that have thus far received little attention and may explain some of the pathological features observed in human disease.

These routes of bacterial invasion require investigation in humans, especially in cases where the etiological agent is known to colonize the nasal mucosa.

In such cases, clinical assessment of olfactory function and the nasal mucosa should be considered. Furthermore, several questions remain unanswered.

We have demonstrated that B. It is unknown if similar mechanisms of transport are used by other bacterial pathogens, such as S.

Second, which bacterial virulence factors are required for penetration of the olfactory epithelium and invasion of the brain via the olfactory and trigeminal nerves?

This review has highlighted the requirement for additional research to characterize the roles of the olfactory and trigeminal nerves in bacterial penetration of the brain and to determine the molecular and cellular mechanisms by which bacterial pathogens may exploit these pathways.

Dando received her Ph. She was subsequently appointed a Postdoctoral Research Fellow at the Institute for Glycomics, Griffith University, and undertook research to investigate the virulence of Burkholderia pseudomallei in a murine model of acute melioidosis.

She recently accepted a postdoctoral research position at Monash University, to research dendritic cell biology in the central nervous system during autoimmune disease.

Alan Mackay-Sim obtained his Ph. He is currently Professor of Neuroscience, Griffith University. With over 30 years of research in the field, Professor Mackay-Sim is a leading expert on the human sense of smell and the biology and development of the olfactory mucosa.

In the last 16 years, he has concentrated on the clinical applications of olfactory cells and their use for neural regeneration therapies, as well as the involvement of the olfactory nerve pathway in the development of disease.

Robert Norton graduated with a degree in medicine in and has worked in a variety of clinical positions, including 5 years in Australian indigenous communities.

He trained in microbiology at the Institute of Medical and Veterinary Science in Adelaide between and He gained an M. In his current capacity as Director of Microbiology at Townsville Hospital, Queensland, Australia, he has collaborated with researchers locally and nationally on projects relating to melioidosis, rheumatic fever, invasive group A streptococcal disease, and Q fever.

Norton is part of the Infectious Diseases and Immunopathogenesis Research Group, which includes clinicians and academic staff of James Cook University.

He has published over peer-reviewed publications and has been successful in obtaining local and national collaborative grants.

His areas of interest include clinical and epidemiological aspects of tropical and emerging infections, development of treatment guidelines, and clinical toxinology.

He initiated the Darwin Prospective Melioidosis Study in , and this remains the basis for ongoing multidisciplinary collaborations on melioidosis.

John obtained his Ph. He then held full-time research fellowships at the University of Melbourne and The University of Queensland.

Since obtaining his Ph. He performs detailed microscopic anatomical studies of the olfactory system and has identified subpopulations of olfactory glia by using live-cell imaging of in vitro cultures.

He is particularly interested in the role of olfactory glia in protecting the brain from bacterial infections. Together with Jenny Ekberg, he recently performed the majority of the work which identified the intranasal route of infection via the olfactory nerve by Burkholderia pseudomallei.

Ekberg obtained her Ph. In , she moved to Griffith University as a Research Fellow and is now focusing on neuron-glia interactions and neural regeneration in the olfactory nervous system.

She continues her work on neural repair and has expanded into the field of bacterial infections of the central nervous system.

Together with James St. John and Ifor Beacham, she recently investigated how B. The focus of Dr. Michael Batzloff obtained his Ph. He has been the recipient of two fellowships from the National Heart Foundation of Australia for his research into vaccine development for Streptococcus pyogenes.

He was subsequently appointed the inaugural Head of the Bacterial Vaccines Laboratory at the Queensland Institute of Medical Research and recently accepted a position at the Institute for Glycomics at Griffith University.

His research interests include neglected tropical diseases, focusing on pathogenesis and vaccine development for the bacterial pathogens Streptococcus pyogenes and Burkholderia pseudomallei.

Ulett is an Associate Professor who received his Ph. He is currently an Australian Research Council ARC Future Fellow in Microbiology at Griffith University, where he leads a research team studying bacterial pathogenesis and the mechanisms of host defense against infection.

His laboratory focuses on infections related to the urogenital tract, programmed cell death, and mechanisms of virulence and disease associated with Escherichia coli , Streptococcus agalactiae , and Burkholderia pseudomallei.

He has been a microbiology researcher in the field of bacterial pathogenesis for 17 years and is a two-time recipient of the George McCracken Infectious Disease Fellow Award from the American Society for Microbiology.

His research program in microbiology and infectious diseases is supported by funding from the National Health and Medical Research Council of Australia.

Beacham undertook undergraduate studies in biochemistry at the University of Otago, New Zealand, and obtained his Ph.

He worked in the general area of molecular microbiology on a variety of bacteria before undertaking work with Burkholderia pseudomallei 16 years ago.

The latter studies were motivated by the endemicity of melioidosis in northern Australia, difficulties with genetic manipulation, and the enigmatic status of B.

He hopes his continuing work will contribute to a greater understanding of the molecular nature of the virulence of B. National Center for Biotechnology Information , U.

Journal List Clin Microbiol Rev v. Author information Copyright and License information Disclaimer. Address correspondence to Glen C.

This article has been cited by other articles in PMC. Meningitis Meningitis, or inflammation of the meninges, is usually acute but can also be subacute and most frequently presents with headache, fever, and neck stiffness Encephalitis In certain circumstances, acute meningitis can be clinically indistinguishable from acute encephalitis, which refers to inflammation of the brain parenchyma in association with neurologic dysfunction Focal Infections The range of focal CNS infections includes brain abscesses, subdural empyema, and epidural abscesses.

Open in a separate window. Immunosurveillance of the CNS The brain parenchyma and spinal cord are populated throughout by resident immune cells, the microglia, which are highly specialized tissue macrophages that are maintained through in situ self-renewal without reconstitution from the bone marrow 81 , — TABLE 1 Known bacterial ligands and their host receptors for adhesion to and invasion of the blood-brain barrier a.

Transcellular Penetration of Brain Microvascular Endothelial Cells Transcellular penetration of brain microvascular endothelial cells, mainly via receptor-mediated mechanisms Fig.

Trojan Horse Penetration of Brain Microvascular Endothelial Cells Bacteria that are capable of surviving within host peripheral immune cells have the ability to invade the CNS via the Trojan horse route.

Protozoa Naegleria fowleri is a free-living amoeba that causes primary amoebic meningoencephalitis, a rare but almost always fatal disease in humans.

Yeasts and Fungi The encapsulated yeast Cryptococcus neoformans is an important cause of fungal meningoencephalitis worldwide and can enter the CNS by penetrating the BBB by use of transcellular, paracellular, and Trojan horse mechanisms following blood-borne dissemination from the lungs as reviewed elsewhere [ ].

The acute aseptic meningitis syndrome. The utility of cerebrospinal fluid parameters in the early microbiological assessment of meningitis.

Encephalitis due to emerging viruses: CNS innate immunity and potential therapeutic targets. Illuminating viral infections in the nervous system.

Causes of encephalitis and differences in their clinical presentations in England: Acute bacterial meningitis in adults.

A review of episodes. Medicine Baltimore, MD Clinical features and independent prognostic factors for acute bacterial meningitis in adults.

Clinical features and prognostic factors in adults with bacterial meningitis. Bacterial meningitis in the United States, The Bacterial Meningitis Study Group.

Bacterial meningitis in the United States, through Bacterial meningitis in the United States, — Trends in bacterial, mycobacterial, and fungal meningitis in England and Wales The spectrum of central nervous system infections in an adult referral hospital in Hanoi, Vietnam.

A history of bacterial meningitis from antiquity to modern times , p 1—16 In Christodoulides M, editor. Ting PL, Norton R. Central nervous system tuberculosis: Pediatric tuberculosis in young children in India: The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat.

Impact of bacteremia on the pathogenesis of experimental pneumococcal meningitis. Routine quantitative blood cultures in children with Haemophilus influenzae or Streptococcus pneumoniae bacteremia.

Relationship between the magnitude of bacteremia in children and the clinical disease. Clinical presentation and prognostic factors of Streptococcus pneumoniae meningitis according to the focus of infection.

Factor H-binding protein is important for meningococcal survival in human whole blood and serum and in the presence of the antimicrobial peptide LL Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival.

The absence of PspA or presence of antibody to PspA facilitates the complement-dependent phagocytosis of pneumococci in vitro.

Pneumolysin with low hemolytic activity confers an early growth advantage to Streptococcus pneumoniae in the blood. Phosphorylcholine allows for evasion of bactericidal antibody by Haemophilus influenzae.

Churchill Livingstone, Philadelphia, PA. Effect of pneumococcal conjugate vaccine on pneumococcal meningitis. Laboratory surveillance of invasive pneumococcal disease in New South Wales, Australia, before and after introduction of 7-valent conjugate vaccine: Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: A decade of invasive meningococcal disease surveillance in Poland.

Epidemiological changes in meningococcal meningitis in Niger from to and the impact of vaccination. Brandtzaeg P, van Deuren M. Classification and pathogenesis of meningococcal infections , p 21—35 In Christodoulides M, editor.

Meningococcal serogroup C conjugate vaccination in England and Wales: Annual report of the Australian Meningococcal Surveillance Programme, E—E [ PubMed ].

Use of an observational cohort study to estimate the effectiveness of the New Zealand group B meningococcal vaccine in children aged under 5 years.

Three-year multicenter surveillance of community-acquired Listeria monocytogenes meningitis in adults. Community-acquired Listeria monocytogenes meningitis in adults.

The changing epidemiology of serious bacterial infections in young infants. Nosocomial meningitis caused by gas producing Klebsiella pneumoniae.

Tuberculous meningitis and miliary tuberculosis: Encephalitis in Australia, Acute measles encephalitis in partially vaccinated adults. The epidemiology and clinical spectrum of melioidosis: The neuropathology of melioidosis: Spinal cord disease due to melioidosis.

Relapsing neurological melioidosis from the top end of the Northern Territory. Neurological melioidosis Burkholderia pseudomallei mimicking Guillain-Barre syndrome.

Cerebral melioidosis in Singapore: Cerebral melioidosis for the first time in the western hemisphere. Clinical characteristics and outcome of brain abscess: Analysis of microbial etiology and mortality in patients with brain abscess.

Anatomy of the meninges: The olfactory route for cerebrospinal fluid drainage into the peripheral lymphatic system. Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species.

Wagshul ME, Johnston M. The brain and the lymphatic system , p — In Santambrogio L, editor. Springer, New York, NY. Blood-brain barrier structure and function and the challenges for CNS drug delivery.

Structure and function of the blood-brain barrier. Engelhardt B, Sorokin L. The blood-brain and the blood-cerebrospinal fluid barriers: Profiling solute carrier transporters in the human blood-brain barrier.

Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. Transcriptomic and quantitative proteomic analysis of transporters and drug metabolizing enzymes in freshly isolated human brain microvessels.

Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: Fluids Barriers CNS 8: Local self-renewal can sustain CNS microglia maintenance and function throughout adult life.

Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Fate mapping analysis reveals that adult microglia derive from primitive macrophages.

Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. CD11c-expressing cells reside in the juxtavascular parenchyma and extend processes into the glia limitans of the mouse nervous system.

The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system.

Flt3L controls the development of radiosensitive dendritic cells in the meninges and choroid plexus of the steady-state mouse brain.

Ransohoff RM, Engelhardt B. The anatomical and cellular basis of immune surveillance in the central nervous system. Localizing central nervous system immune surveillance: Engelhardt B, Ransohoff RM.

Matrix metalloprotease 8-dependent extracellular matrix cleavage at the blood-CSF barrier contributes to lethality during systemic inflammatory diseases.

Brain-blood barrier breakdown and pro-inflammatory mediators in neonate rats submitted meningitis by Streptococcus pneumoniae. Inducible nitric oxide synthase mediates hippocampal caspase-3 activation in pneumococcal meningitis.

A model of brain tissue damage in Streptococcus pneumoniae meningitis. Access to detailed statistics of competitions, atheletes, horses and events.

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