Virulence Factors of Meningitis-Causing Bacteria: Enabling Brain Entry across the Blood–Brain Barrier
Open accessAbstract
Infections of the central nervous system (CNS) are still a major cause of morbidity and mortality worldwide. Traversal of the barriers protecting the brain by pathogens is a prerequisite for the development of meningitis. Bacteria have developed a variety of different strategies to cross these barriers and reach the CNS. To this end, they use a variety of different virulence factors that enable them to attach to and traverse these barriers. These virulence factors mediate adhesion to and invasion into host cells, intracellular survival, induction of host cell signaling and inflammatory response, and affect barrier function. While some of these mechanisms differ, others are shared by multiple pathogens. Further understanding of these processes, with special emphasis on the difference between the blood–brain barrier and the blood–cerebrospinal fluid barrier, as well as virulence factors used by the pathogens, is still needed.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Detection of enteroviral RNA in the CSF is a direct indicator of CNS involvement.
“The detection of enteroviral RNA in the CSF is therefore a direct indicator of CNS involvement (23–25).”
From Pathogen detection in acellular cerebrospinal fluid: diagnostic insights from a pediatric cohort in Colombia (2026) · cites this paper as [25]
The Introduction discusses diagnosing bacterial meningitis by the presence of bacteria in the CNS, but does not address enteroviruses. Searches for enteroviral RNA in CSF and for enterovirus-related diagnosis found no passage stating that its detection indicates CNS involvement. (LLM, conf=0.78)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Blood-Brain Barrier: From Physiology to Disease and Back
Sweeney, M. D., Zhao, Z., Montagne, A., Nelson, A. R., & Zlokovic, B. V. (2019) · Physiological Reviews · doi:10.1152/physrev.00050.2017 · Cited by 2,294 · cited 1× · see citing works
“Transporter systems of the BBB include solute carrier-mediated transport, receptor-mediated transport, as well as active efflux and ion transport [14].”
BackgroundBacterial Adhesion and Entry into Host Cells
Pizarro-Cerdá, J., & Cossart, P. (2006) · Cell · doi:10.1016/j.cell.2006.02.012 · Cited by 977 · cited 1× · see citing works
“Furthermore, replication and persistence inside host cells has been demonstrated for a variety of meningitis-causing pathogens as well [36].”
BackgroundEpidemiology, Diagnosis, and Antimicrobial Treatment of Acute Bacterial Meningitis
Brouwer, M. C., Tunkel, A. R., & van de Beek, D. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00070-09 · Cited by 930 · see citing works
Watt, J. P., Wolfson, L. J., O'Brien, K. L., Henkle, E., Deloria-Knoll, M., McCall, N., Lee, E., Levine, O. S., Hajjeh, R., Mulholland, K., et al. (2009) · The Lancet · doi:10.1016/s0140-6736(09)61203-4 · Cited by 501 · see citing works
Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules
Cress, B. F., Englaender, J. A., He, W., Kasper, D., Linhardt, R. J., & Koffas, M. A. G. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12056 · Cited by 282 · see citing works
Doran, K. S., Engelson, E. J., Khosravi, A., Maisey, H. C., Fedtke, I., Equils, O., Michelsen, K. S., Arditi, M., Peschel, A., & Nizet, V. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23829 · Cited by 231 · see citing works
Weller, R. O., Sharp, M. M., Christodoulides, M., Carare, R. O., & Møllgård, K. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1809-z · Cited by 222 · cited 1× · see citing works
“Another major barrier protecting the brain is the BCSFB, which can be separated into a barrier to the inner CSF in the ventricles at the choroid plexus (CP) and barriers to the outer CSF located at the arachnoidea and blood vessels present in the subarachnoidal space [15].”
BackgroundSaunders, N. R., Habgood, M. D., Møllgård, K., & Dziegielewska, K. M. (2016) · F1000Research · doi:10.12688/f1000research.7378.1 · Cited by 143 · see citing works
Banerjee, A., Kim, B. J., Carmona, E. M., Cutting, A. S., Gurney, M. A., Carlos, C., Feuer, R., Prasadarao, N. V., & Doran, K. S. (2011) · Nature Communications · doi:10.1038/ncomms1474 · Cited by 142 · see citing works
Deng, L., Spencer, B. L., Holmes, J. A., Mu, R., Rego, S., Weston, T. A., Hu, Y., Sanches, G. F., Yoon, S., Park, N., et al. (2019) · PLOS Pathogens · doi:10.1371/journal.ppat.1007848 · Cited by 74 · see citing works
Flagged first, then by citations
Research works printed but not linked: 186
- [1]Dando S.J. Mackay-Sim A. Norton R. Currie B.J. St John J.A. Ekberg J.A.K. Batzloff M. Ulett G.C. Beacham I.R. Pathogens penetrating the central nervous system: Infection pathways and the cellular and molecular mechanisms of invasion Clin. Microbiol. Rev. 2014 27 691 726 10.1128/CMR.00118-13 25278572 PMC4187632 · DOI · Paper page
- [2]Kim K.S. Mechanisms of microbial traversal of the blood-brain barrier Nat. Rev. Microbiol. 2008 6 625 634 10.1038/nrmicro1952 18604221 PMC5206914 · DOI
- [3]Wolburg H. Paulus W. Choroid plexus: Biology and pathology Acta Neuropathol. 2010 119 75 88 20033190
- [4]Doran K.S. Fulde M. Gratz N. Kim B.J. Nau R. Prasadarao N. Schubert-Unkmeir A. Tuomanen E.I. Valentin-Weigand P. Host-pathogen interactions in bacterial meningitis Acta Neuropathol. 2016 131 185 209 10.1007/s00401-015-1531-z 26744349 PMC4713723 · DOI · Paper page
- [5]Marques F. Sousa J.C. Sousa N. Palha J.A. Blood-brain-barriers in aging and in alzheimer‘s disease Mol. Neurodegener. 2013 8 38 24148264 PMC4015275
- [7]Lauer A.N. Tenenbaum T. Schroten H. Schwerk C. The diverse cellular responses of the choroid plexus during infection of the central nervous system Am. J. Physiol. Cell Physiol. 2018 314 C152 C165 29070490
- [8]Van Sorge N.M. Doran K.S. Defense at the border: The blood-brain barrier versus bacterial foreigners Future Microbiol. 2012 7 383 394 22393891 PMC3589978
- [9]Daneman R. Prat A. The blood-brain barrier Cold Spring Harb. Perspect. Biol. 2015 7 10.1101/cshperspect.a020412 PMC4292164 25561720 · DOI · Paper page
- [10]Abbott N.J. Patabendige A.A.K. Dolman D.E.M. Yusof S.R. Begley D.J. Structure and function of the blood-brain barrier Neurobiol. Dis. 2010 37 13 25 10.1016/j.nbd.2009.07.030 19664713 · DOI · Paper page
- [11]Dias M.C. Coisne C. Lazarevic I. Baden P. Hata M. Iwamoto N. Francisco D.M.F. Vanlandewijck M. He L.Q. Baier F.A. Claudin-3-deficient c57bl/6j mice display intact brain barriers Sci. Rep. 2019 9 203 10.1038/s41598-018-36731-3 30659216 PMC6338742 · DOI
- [12]Tietz S. Engelhardt B. Brain barriers: Crosstalk between complex tight junctions and adherens junctions J. Cell Biol. 2015 209 493 506 10.1083/jcb.201412147 26008742 PMC4442813 · DOI · Paper page
- [13]Hawkins R.A. O’Kane R.L. Simpson I.A. Vina J.R. Structure of the blood-brain barrier and its role in the transport of amino acids J. Nutr. 2006 136 218s 226s 10.1093/jn/136.1.218S 16365086 · DOI · Paper page
- [16]Liddelow S.A. Development of the choroid plexus and blood-csf barrier Front. Neurosci. 2015 9 10.3389/fnins.2015.00032 PMC4347429 25784848 · DOI
- [17]Schwerk C. Tenenbaum T. Kim K.S. Schroten H. The choroid plexus-a multi-role player during infectious diseases of the cns Front. Cell. Neurosci. 2015 9 10.3389/fncel.2015.00080 PMC4357259 25814932 · DOI · Paper page
- [18]Bernd A. Ott M. Ishikawa H. Schroten H. Schwerk C. Fricker G. Characterization of efflux transport proteins of the human choroid plexus papilloma cell line hibcpp, a functional in vitro model of the blood-cerebrospinal fluid barrier Pharm. Res. 2015 32 2973 2982 10.1007/s11095-015-1679-1 25986174 · DOI
- [19]Ransohoff R.M. Engelhardt B. The anatomical and cellular basis of immune surveillance in the central nervous system Nat. Rev. Immunol. 2012 12 623 635 10.1038/nri3265 22903150 · DOI
- [20]Sullivan T.D. Lascolea L.J. Neter E. Relationship between the magnitude of bacteremia in children and the clinical-disease Pediatrics 1982 69 699 702 6804923
- [21]Dietzman D.E. Fischer G.W. Schoenknecht F.D. Neonatal escherichia coli septicemia--bacterial counts in blood J. Pediatr. 1974 85 128 130 10.1016/S0022-3476(74)80308-2 4604810 · DOI
- [22]Kim K.S. Human meningitis-associated escherichia coli Ecosal Plus 2016 7 10.1128/ecosalplus.ESP-0015-2015 27223820 PMC4881430 · DOI · Paper page
- [23]Bell L.M. Alpert G. Campos J.M. Plotkin S.A. Routine quantitative blood cultures in children with haemophilus influenzae or streptococcus pneumoniae bacteremia Pediatrics 1985 76 901 904 3877910
- [24]Virji M. Ins and outs of microbial adhesion Top. Curr. Chem. 2009 288 139 156 22328029
- [25]Cossart P. Helenius A. Endocytosis of viruses and bacteria Cold Spring Harb. Perspect. Biol. 2014 6 a016972 10.1101/cshperspect.a016972 25085912 PMC4107984 · DOI
- [26]Cossart P. Sansonetti P.J. Bacterial invasion: The paradigms of enteroinvasive pathogens Science 2004 304 242 248 10.1126/science.1090124 15073367 · DOI
- [27]Mota L.J. Cornelis G.R. The bacterial injection kit: Type iii secretion systems Ann. Med. 2005 37 234 249 10.1080/07853890510037329 16019722 · DOI
- [28]Santiago-Tirado F.H. Doering T.L. False friends: Phagocytes as trojan horses in microbial brain infections PLoS Path. 2017 13 e1006680 10.1371/journal.ppat.1006680 PMC5730104 29240825 · DOI
- [29]Selbach M. Backert S. Cortactin: An achilles’ heel of the actin cytoskeleton targeted by pathogens Trends Microbiol. 2005 13 181 189 10.1016/j.tim.2005.02.007 15817388 · DOI
- [30]Stradal T.E.B. Schelhaas M. Actin dynamics in host-pathogen interaction Febs Lett. 2018 592 3658 3669 10.1002/1873-3468.13173 29935019 PMC6282728 · DOI
- [31]Frischknecht F. Way M. Surfing pathogens and the lessons learned for actin polymerization Trends Cell Biol. 2001 11 30 38 10.1016/S0962-8924(00)01871-7 11146296 · DOI
- [32]Lamason R.L. Welch M.D. Actin-based motility and cell-to-cell spread of bacterial pathogens Curr. Opin. Microbiol. 2017 35 48 57 10.1016/j.mib.2016.11.007 27997855 PMC5474209 · DOI
- [33]Borkowski J. Li L. Steinmann U. Quednau N. Stump-Guthier C. Weiss C. Findeisen P. Gretz N. Ishikawa H. Tenenbaum T. Neisseria meningitidis elicits a pro-inflammatory response involving ikappabzeta in a human blood-cerebrospinal fluid barrier model J. Neuroinflammation 2014 11 163 10.1186/s12974-014-0163-x 25347003 PMC4172843 · DOI
- [34]Dinner S. Kaltschmidt J. Stump-Guthier C. Hetjens S. Ishikawa H. Tenenbaum T. Schroten H. Schwerk C. Mitogen-activated protein kinases are required for effective infection of human choroid plexus epithelial cells by listeria monocytogenes Microbes Infect. 2017 19 18 33 10.1016/j.micinf.2016.09.003 27671041 · DOI
- [35]Krachler A.M. Woolery A.R. Orth K. Manipulation of kinase signaling by bacterial pathogens J. Cell Biol. 2011 195 1083 1092 10.1083/jcb.201107132 22123833 PMC3246894 · DOI
- [37]Wang S. Peng L. Gai Z. Zhang L. Jong A. Cao H. Huang S.H. Pathogenic triad in bacterial meningitis: Pathogen invasion, nf-kappab activation, and leukocyte transmigration that occur at the blood-brain barrier Front. Microbiol 2016 7 148 10.3389/fmicb.2016.00148 26925035 PMC4760054 · DOI
- [39]Koedel U. Scheld W.M. Pfister H.W. Pathogenesis and pathophysiology of pneumococcal meningitis Lancet Infect. Dis. 2002 2 721 736 10.1016/S1473-3099(02)00450-4 12467688 · DOI
- [40]Kim S.Y. Buckwalter M. Soreq H. Vezzani A. Kaufer D. Blood-brain barrier dysfunction-induced inflammatory signaling in brain pathology and epileptogenesis Epilepsia 2012 53 37 44 10.1111/j.1528-1167.2012.03701.x 23134494 PMC3703535 · DOI · Paper page
- [41]Haberl R.L. Anneser F. Kodel U. Pfister H.W. Is nitric-oxide involved as a mediator of cerebrovascular changes in the early phase of experimental pneumococcal meningitis Neurol. Res. 1994 16 108 112 10.1080/01616412.1994.11740205 7913993 · DOI
- [42]Leppert D. Leib S.L. Grygar C. Miller K.M. Schaad U.B. Hollander G.A. Matrix metalloproteinase (mmp)-8 and mmp-9 in cerebrospinal fluid during bacterial meningitis: Association with blood-brain barrier damage and neurological sequelae Clin. Infect. Dis. 2000 31 80 84 10.1086/313922 10913401 · DOI
- [43]Zwijnenburg P.J. de Bie H.M. Roord J.J. van der Poll T. van Furth A.M. Chemotactic activity of cxcl5 in cerebrospinal fluid of children with bacterial meningitis J. Neuroimmunol. 2003 145 148 153 10.1016/j.jneuroim.2003.09.013 14644041 · DOI
- [44]Azuma H. Tsuda N. Sasaki K. Okuno A. Clinical significance of cytokine measurement for detection of meningitis J. Pediatr 1997 131 463 465 10.1016/S0022-3476(97)80079-0 9329430 · DOI
- [45]Coutinho L.G. Grandgirard D. Leib S.L. Agnez-Lima L.F. Cerebrospinal-fluid cytokine and chemokine profile in patients with pneumococcal and meningococcal meningitis BMC Infect. Dis. 2013 13 326 10.1186/1471-2334-13-326 23865742 PMC3717124 · DOI
- [47]Hauser S. Wegele C. Stump-Guthier C. Borkowski J. Weiss C. Rohde M. Ishikawa H. Schroten H. Schwerk C. Adam R. Capsule and fimbriae modulate the invasion of haemophilus influenzae in a human blood-cerebrospinal fluid barrier model Int. J. Med. Microbiol. 2018 308 829 839 10.1016/j.ijmm.2018.07.004 30049648 · DOI
- [48]Schwerk C. Papandreou T. Schuhmann D. Nickol L. Borkowski J. Steinmann U. Quednau N. Stump C. Weiss C. Berger J. Polar invasion and translocation of neisseria meningitidis and streptococcus suis in a novel human model of the blood-cerebrospinal fluid barrier PLoS ONE 2012 7 e30069 10.1371/journal.pone.0030069 22253884 PMC3256222 · DOI
- [49]Gendrin C. Merillat S. Vornhagen J. Coleman M. Armistead B. Ngo L. Aggarwal A. Quach P. Berrigan J. Rajagopal L. Diminished capsule exacerbates virulence, blood-brain barrier penetration, intracellular persistence, and antibiotic evasion of hyperhemolytic group b streptococci J. Infect. Dis. 2018 217 1128 1138 10.1093/infdis/jix684 29301010 PMC5939829 · DOI
- [50]Wu Z.F. Wu C.Y. Shao J. Zhu Z.Z. Wang W.X. Zhang W.W. Tang M. Pei N. Fan H.J. Li J.G. The streptococcus suis transcriptional landscape reveals adaptation mechanisms in pig blood and cerebrospinal fluid RNA 2014 20 882 898 10.1261/rna.041822.113 24759092 PMC4024642 · DOI
- [51]Al-Obaidi M.M.J. Desa M.N.M. Mechanisms of blood brain barrier disruption by different types of bacteria, and bacterial-host interactions facilitate the bacterial pathogen invading the brain Cell. Mol. Neurobiol. 2018 38 1349 1368 10.1007/s10571-018-0609-2 30117097 PMC11481977 · DOI
- [52]Disson O. Lecuit M. Targeting of the central nervous system by listeria monocytogenes Virulence 2012 3 213 221 10.4161/viru.19586 22460636 PMC3396700 · DOI
- [53]Radoshevich L. Cossart P. Listeria monocytogenes: Towards a complete picture of its physiology and pathogenesis Nat. Rev. Microbiol. 2018 16 32 46 10.1038/nrmicro.2017.126 29176582 · DOI
- [54]Drevets D.A. Leenen P.J.M. Greenfield R.A. Invasion of the central nervous system by intracellular bacteria Clin. Microbiol. Rev. 2004 17 323 347 10.1128/CMR.17.2.323-347.2004 15084504 PMC387409 · DOI
- [55]Pagelow D. Chhatbar C. Beineke A. Liu X.K. Nerlich A. van Vorst K. Rohde M. Kalinke U. Forster R. Halle S. The olfactory epithelium as a port of entry in neonatal neurolisteriosis Nat. Commun. 2018 9 4269 10.1038/s41467-018-06668-2 30323282 PMC6189187 · DOI
- [56]Greiffenberg L. Goebel W. Kim K.S. Daniels J. Kuhn M. Interaction of listeria monocytogenes with human brain microvascular endothelial cells: An electron microscopic study Infect. Immun. 2000 68 3275 3279 10.1128/IAI.68.6.3275-3279.2000 10816473 PMC97578 · DOI
- [57]Grundler T. Quednau N. Stump C. Orian-Rousseau V. Ishikawa H. Wolburg H. Schroten H. Tenenbaum T. Schwerk C. The surface proteins inla and inlb are interdependently required for polar basolateral invasion by listeria monocytogenes in a human model of the blood-cerebrospinal fluid barrier Microbes Infect. 2013 15 291 301 10.1016/j.micinf.2012.12.005 23376167 · DOI
- [58]Ghosh P. Halvorsen E.M. Ammendolia D.A. Mor-Vaknin N. O’Riordan M.X.D. Brumell J.H. Markovitz D.M. Higgins D.E. Invasion of the brain by listeria monocytogenes is mediated by inlf and host cell vimentin MBio 2018 9 10.1128/mBio.00160-18 PMC5829824 29487235 · DOI
- [59]Tang P. Rosenshine I. Finlay B.B. Listeria-monocytogenes, an invasive bacterium, stimulates map kinase upon attachment to epithelial-cells Mol. Biol. Cell 1994 5 455 464 10.1091/mbc.5.4.455 8054686 PMC301054 · DOI
- [60]Tang P. Sutherland C.L. Gold M.R. Finlay B.B. Listeria monocytogenes invasion of epithelial cells requires the mek-1/erk-2 mitogen-activated protein kinase pathway Infect. Immun. 1998 66 1106 1112 9488402 PMC108022
- [61]Pizarro-Cerda J. Kuhbacher A. Cossart P. Entry of listeria monocytogenes in mammalian epithelial cells: An updated view Cold Spring Harb. Perspect. Med. 2012 2 a010009 10.1101/cshperspect.a010009 23125201 PMC3543101 · DOI
- [62]Veiga E. Cossart P. Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells Nat. Cell Biol. 2005 7 10.1038/ncb1292 16113677 · DOI
- [63]Veiga E. Guttman J.A. Bonazzi M. Boucrot E. Toledo-Arana A. Lin A.E. Enninga J. Pizarro-Cerda J. Finlay B.B. Kirchhausen T. Invasive and adherent bacterial pathogens co-opt host clathrin for infection Cell Host Microbe 2007 2 340 351 10.1016/j.chom.2007.10.001 18005755 PMC2803069 · DOI
- [64]Kayal S. Lilienbaum A. Join-Lambert O. Li X.X. Israel A. Berche P. Listeriolysin o secreted by listeria monocytogenes induces nf-kappa b signalling by activating the i kappa b kinase complex Mol. Microbiol. 2002 44 1407 1419 10.1046/j.1365-2958.2002.02973.x 12028384 · DOI
- [65]Tang P. Rosenshine I. Cossart P. Finlay B.B. Listeriolysin o activates mitogen-activated protein kinase in eucaryotic cells Infect. Immun. 1996 64 2359 2361 8675352 PMC174081
- [66]Weiglein I. Goebel W. Troppmair J. Rapp U.R. Demuth A. Kuhn M. Listeria monocytogenes infection of hela cells results in listeriolysin o-mediated transient activation of the raf-mek-map kinase pathway Fems Microbiol. Lett. 1997 148 189 195 10.1111/j.1574-6968.1997.tb10287.x 9084147 · DOI
- [67]Lambrechts A. Gevaert K. Cossart P. Vandekerckhove J. Van Troys M. Listeria comet tails: The actin-based motility machinery at work Trends Cell Biol. 2008 18 220 227 10.1016/j.tcb.2008.03.001 18396046 · DOI
- [68]Kocks C. Gouin E. Tabouret M. Berche P. Ohayon H. Cossart P. L-monocytogenes-induced actin assembly requires the acta gene-product, a surface protein Cell 1992 68 521 531 10.1016/0092-8674(92)90188-I 1739966 · DOI · Paper page
- [69]Gouin E. Adib-Conquy M. Balestrino D. Nahori M.A. Villiers V. Colland F. Dramsi S. Dussurget O. Cossart P. The listeria monocytogenes inlc protein interferes with innate immune responses by targeting the i kappa b kinase subunit ikk alpha Proc. Natl. Acad. Sci. USA 2010 107 17333 17338 10.1073/pnas.1007765107 20855622 PMC2951401 · DOI
- [70]Rajabian T. Gavicherla B. Heisig M. Muller-Altrock S. Goebel W. Gray-Owen S.D. Ireton K. The bacterial virulence factor inlc perturbs apical cell junctions and promotes cell-to-cell spread of listeria Nat. Cell Biol. 2009 11 1212 1218 10.1038/ncb1964 19767742 PMC2755649 · DOI
- [71]Gottschalk M. Xu J.G. Calzas C. Segura M. Streptococcus suis: A new emerging or an old neglected zoonotic pathogen? Future Microbiol. 2010 5 371 391 10.2217/fmb.10.2 20210549 · DOI
- [72]Tenenbaum T. Papandreou T. Gellrich D. Friedrichs U. Seibt A. Adam R. Wewer C. Galla H.J. Schwerk C. Schroten H. Polar bacterial invasion and translocation of streptococcus suis across the blood-cerebrospinal fluid barrier in vitro Cell. Microbiol. 2009 11 323 336 10.1111/j.1462-5822.2008.01255.x 19046337 · DOI
- [73]Vanier G. Segura M. Gottschalk M. Characterization of the invasion of porcine endothelial cells by streptococcus suis serotype 2 Can. J. Vet. Res. Rev. Can. De Rech. Vet. 2007 71 81 89 PMC1829181 17479770
- [74]Benga L. Goethe R. Rohde M. Valentin-Weigand P. Non-encapsulated strains reveal novel insights in invasion and survival of streptococcus suis in epithelial cells Cell. Microbiol. 2004 6 867 881 10.1111/j.1462-5822.2004.00409.x 15272867 · DOI
- [75]Willenborg J. Fulde M. de Greeff A. Rohde M. Smith H.E. Valentin-Weigand P. Goethe R. Role of glucose and ccpa in capsule expression and virulence of streptococcus suis Microbiology 2011 157 1823 1833 10.1099/mic.0.046417-0 21349980 · DOI
- [76]Charland N. Nizet V. Rubens C.E. Kim K.S. Lacouture S. Gottschalk M. Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells Infect. Immun. 2000 68 637 643 10.1128/IAI.68.2.637-643.2000 10639427 PMC97186 · DOI
- [77]Benga L. Friedl P. Valentin-Weigand P. Adherence of streptococcus suis to porcine endothelial cells J. Vet. Med. Ser. B-Infect. Dis. Vet. Public Health 2005 52 392 395 10.1111/j.1439-0450.2005.00880.x 16283918 · DOI
- [78]Vanier G. Segura M. Friedl P. Lacouture S. Gottschalk M. Invasion of porcine brain microvascular endothelial cells by streptococcus suis serotype 2 Infect. Immun. 2004 72 1441 1449 10.1128/IAI.72.3.1441-1449.2004 14977949 PMC356020 · DOI
- [79]Fittipaldi N. Segura M. Grenier D. Gottschalk M. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent streptococcus suis Future Microbiol. 2012 7 259 279 10.2217/fmb.11.149 22324994 · DOI
- [80]Sun Y. Li N. Zhang J. Liu H. Liu J. Xia X. Sun C. Feng X. Gu J. Du C. Enolase of streptococcus suis serotype 2 enhances blood-brain barrier permeability by inducing il-8 release Inflammation 2016 39 718 726 10.1007/s10753-015-0298-7 26732390 · DOI
- [81]Lun S.C. Perez-Casal J. Connor W. Willson P.J. Role of suilysin in pathogenesis of streptococcus suis capsular serotype 2 Microb. Pathog. 2003 34 27 37 10.1016/S0882-4010(02)00192-4 12620382 · DOI
- [82]Seitz M. Baums C.G. Neis C. Benga L. Fulde M. Rohde M. Goethe R. Valentin-Weigand P. Subcytolytic effects of suilysin on interaction of streptococcus suis with epithelial cells Vet. Microbiol. 2013 167 584 591 10.1016/j.vetmic.2013.09.010 24095145 · DOI
- [83]Vadeboncoeur N. Segura M. Al-Numani D. Vanier G. Gottschalk M. Pro-inflammatory cytokine and chemokine release by human brain microvascular endothelial cells stimulated by streptococcus suis serotype 2 Fems Immunol. Med. Microbiol. 2003 35 49 58 10.1111/j.1574-695X.2003.tb00648.x 12589957 · DOI
- [84]Tenenbauma T. Matalon D. Adam R. Seibt A. Wewer C. Schwerk C. Galla H.J. Schrotena H. Dexamethasone prevents alteration of tight junction-associated proteins and barrier function in porcine choroid plexus epithelial cells after infection with streptococcus suis in vitro Brain Res. 2008 1229 1 17 10.1016/j.brainres.2008.06.118 18644352 · DOI
- [85]Wewer C. Seibt A. Wolburg H. Greune L. Schmidt M.A. Berger J. Galla H.J. Quitsch U. Schwerk C. Schroten H. Transcellular migration of neutrophil granulocytes through the blood-cerebrospinal fluid barrier after infection with streptococcus suis J. Neuroinflammation 2011 8 51 10.1186/1742-2094-8-51 21592385 PMC3120695 · DOI
- [86]Scarborough M. Thwaites G.E. The diagnosis and management of acute bacterial meningitis in resource-poor settings Lancet Neurol. 2008 7 637 648 10.1016/S1474-4422(08)70139-X 18565457 · DOI
- [87]Iovino F. Orihuela C.J. Moorlag H.E. Molema G. Bijlsma J.J.E. Interactions between blood-borne streptococcus pneumoniae and the blood-brain barrier preceding meningitis PLoS ONE 2013 8 e68408 10.1371/journal.pone.0068408 23874613 PMC3713044 · DOI
- [88]Van Ginkel F.W. McGhee J.R. Watt J.M. Campos-Torres A. Parish L.A. Briles D.E. Pneumococcal carriage results in ganglioside-mediated olfactory tissue infection (vol 100, pg 14363, 2003) Proc. Natl. Acad. Sci. USA 2004 101 6834 PMC283597 14610280
- [89]Wartha F. Beiter K. Albiger B. Fernebro J. Zychlinsky A. Normark S. Henriques-Normark B. Capsule and d-alanylated lipoteichoic acids protect streptococcus pneumoniae against neutrophil extracellular traps Cell. Microbiol. 2007 9 1162 1171 10.1111/j.1462-5822.2006.00857.x 17217430 · DOI
- [90]Middleton D.R. Paschall A.V. Duke J.A. Avci F.Y. Enzymatic hydrolysis of pneumococcal capsular polysaccharide renders the bacterium vulnerable to host defense Infect. Immun. 2018 86 10.1128/IAI.00316-18 PMC6056847 29866907 · DOI
- [91]Keller L.E. Jones C.V. Thornton J.A. Sanders M.E. Swiatlo E. Nahm M.H. Park I.H. McDaniel L.S. Pspk of streptococcus pneumoniae increases adherence to epithelial cells and enhances nasopharyngeal colonization Infect. Immun. 2013 81 173 181 10.1128/IAI.00755-12 23115034 PMC3536125 · DOI
- [92]Li-Korotky H.S. Lo C.Y. Banks J.M. Interaction of pneumococcal phase variation, host and pressure/gas composition: Virulence expression of nana, hyla, pspa and cbpa in simulated otitis media Microb. Pathog. 2010 49 204 210 10.1016/j.micpath.2010.05.014 20576489 · DOI
- [93]Shainheit M.G. Muie M. Camilli A. The core promoter of the capsule operon of streptococcus pneumoniae is necessary for colonization and invasive disease Infect. Immun. 2014 82 694 705 10.1128/IAI.01289-13 24478084 PMC3911406 · DOI
- [94]Iovino F. Molema G. Bijlsma J.J.E. Platelet endothelial cell adhesion molecule-1, a putative receptor for the adhesion of streptococcus pneumoniae to the vascular endothelium of the blood-brain barrier Infect. Immun. 2014 82 3555 3566 10.1128/IAI.00046-14 24914219 PMC4187830 · DOI
- [95]Uchiyama S. Carlin A.F. Khosravi A. Weiman S. Banerjee A. Quach D. Hightower G. Mitchell T.J. Doran K.S. Nizet V. The surface-anchored nana protein promotes pneumococcal brain endothelial cell invasion J. Exp. Med. 2009 206 1845 1852 10.1084/jem.20090386 19687228 PMC2737157 · DOI
- [96]Gratz N. Loh L.N. Mann B. Gao G. Carter R. Rosch J. Tuomanen E.I. Pneumococcal neuraminidase activates tgf-beta signalling Microbiology 2017 163 1198 1207 28749326 PMC5817201
- [97]Iovino F. Engelen-Lee J.Y. Brouwer M. van de Beek D. van der Ende A. Seron M.V. Mellroth P. Muschiol S. Bergstrand J. Widengren J. Pigr and pec am-1 bind to pneumococcal adhesins rrga and pspc mediating bacterial brain invasion J. Exp. Med. 2017 214 1619 1630 10.1084/jem.20161668 28515075 PMC5461002 · DOI
- [98]Bagnoli F. Moschioni M. Donati C. Dimitrovska V. Ferlenghi I. Facciotti C. Muzzi A. Giusti F. Emolo C. Sinisi A. A second pilus type in streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells J. Bacteriol. 2008 190 5480 5492 10.1128/JB.00384-08 18515415 PMC2493256 · DOI
- [99]Orihuela C.J. Mahdavi J. Thornton J. Mann B. Wooldridge K.G. Abouseada N. Oldfield N.J. Self T. Ala’Aldeen D.A. Tuomanen E.I. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models J. Clin. Invest. 2009 119 1638 1646 10.1172/JCI36759 19436113 PMC2689107 · DOI · Paper page
- [100]Schmidt F. Kakar N. Meyer T.C. Depke M. Masouris I. Burchhardt G. Gomez-Mejia A. Dhople V. Havarstein L.S. Sun Z. In vivo proteomics identifies the competence regulon and alib oligopeptide transporter as pathogenic factors in pneumococcal meningitis PLoS Path. 2019 15 e1007987 10.1371/journal.ppat.1007987 PMC6687184 31356624 · DOI
- [101]Chen J.Q. Li N.N. Wang B.W. Liu X.F. Liu J.L. Chang Q. Upregulation of cbp by ply can cause permeability of blood-brain barrier to increase meningitis J. Biochem. Mol. Toxicol. 2019 e22333 10.1002/jbt.22333 30980515 · DOI
- [102]Zysk G. Schneider-Wald B.K. Hwang J.H. Bejo L. Kim K.S. Mitchell T.J. Hakenbeck R. Heinz H.P. Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by streptococcus pneumoniae Infect. Immun. 2001 69 845 852 10.1128/IAI.69.2.845-852.2001 11159977 PMC97961 · DOI
- [103]Mandi L.K. Wang H. Van der Hoek M.B. Paton J.C. Ogunniyi A.D. Identification of a novel pneumococcal vaccine antigen preferentially expressed during meningitis in mice J. Clin. Invest. 2012 122 2208 2220 22622042 PMC3366392
- [104]Wang Y. Liu X. Liu Q. Nod2 expression in streptococcus pneumoniae meningitis and its influence on the blood-brain barrier Can. J. Infect. Dis Med. Microbiol 2018 2018 10.1155/2018/7292084 30186539 PMC6109993 · DOI
- [105]Barichello T. Fagundes G.D. Generoso J.S. Moreira A.P. Costa C.S. Zanatta J.R. Simoes L.R. Petronilho F. Dal-Pizzol F. Vilela M.C. Brain-blood barrier breakdown and pro-inflammatory mediators in neonate rats submitted meningitis by streptococcus pneumoniae Brain Res. 2012 1471 162 168 10.1016/j.brainres.2012.06.054 22796596 · DOI
- [107]Jones N. Bohnsack J.F. Takahashi S. Oliver K.A. Chan M.S. Kunst F. Glaser P. Rusniok C. Crook D.W.M. Harding R.M. Multilocus sequence typing system for group b streptococcus J. Clin. Microbiol. 2003 41 2530 2536 10.1128/JCM.41.6.2530-2536.2003 12791877 PMC156480 · DOI
- [108]Maisey H.C. Doran K.S. Nizet V. Recent advances in understanding the molecular basis of group b streptococcus virulence Expert Rev. Mol. Med. 2008 10 e27 10.1017/S1462399408000811 18803886 PMC2676346 · DOI
- [109]Nizet V. Kim K.S. Stins M. Jonas M. Chi E.Y. Nguyen D. Rubens C.E. Invasion of brain microvascular endothelial cells by group b streptococci Infect. Immun. 1997 65 5074 5081 9393798 PMC175731
- [110]Tazi A. Disson O. Bellais S. Bouaboud A. Dmytruk N. Dramsi S. Mistou M.Y. Khun H. Mechler C. Tardieux I. The surface protein hvga mediates group b streptococcus hypervirulence and meningeal tropism in neonates J. Exp. Med. 2010 207 2313 2322 10.1084/jem.20092594 20956545 PMC2964583 · DOI
- [111]Lauer P. Rinaudo C.D. Soriani M. Margarit I. Maione D. Rosini R. Taddei A.R. Mora M. Rappuoli R. Grandi G. Genome analysis reveals pili in group b streptococcus Science 2005 309 105 10.1126/science.1111563 15994549 · DOI
- [112]Maisey H.C. Hensler M. Nizet V. Doran K.S. Group b streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells J. Bacteriol. 2007 189 1464 1467 10.1128/JB.01153-06 17041051 PMC1797338 · DOI
- [113]Mu R. Kim B.J. Paco C. Del Rosario Y. Courtney H.S. Doran K.S. Identification of a group b streptococcal fibronectin binding protein, sfba, that contributes to invasion of brain endothelium and development of meningitis Infect. Immun. 2014 82 2276 2286 10.1128/IAI.01559-13 24643538 PMC4019170 · DOI
- [114]Seo H.S. Mu R. Kim B.J. Doran K.S. Sullam P.M. Binding of glycoprotein srr1 of streptococcus agalactiae to fibrinogen promotes attachment to brain endothelium and the development of meningitis PLoS Path. 2012 8 e1002947 10.1371/journal.ppat.1002947 23055927 PMC3464228 · DOI · Paper page
- [116]Shin S. Maneesh P.S. Lee J.S. Romer L.H. Kim K.S. Focal adhesion kinase is involved in type iii group b streptococcal invasion of human brain microvascular endothelial cells Microb. Pathog. 2006 41 168 173 10.1016/j.micpath.2006.07.003 16949788 · DOI
- [118]Luo S. Cao Q. Ma K. Wang Z.F. Liu G.J. Lu C.P. Liu Y.J. Quantitative assessment of the blood-brain barrier opening caused by streptococcus agalactiae hyaluronidase in a balb/c mouse model Sci Rep.-Uk 2017 7 13529 10.1038/s41598-017-13234-1 PMC5648924 29051603 · DOI
- [119]Kim B.J. McDonagh M.A. Deng L. Gastfriend B.D. Schubert-Unkmeir A. Doran K.S. Shusta E.V. Streptococcus agalactiae disrupts p-glycoprotein function in brain endothelial cells Fluids Barriers Cns 2019 16 1 10 10.1186/s12987-019-0146-5 31434575 PMC6704684 · DOI
- [120]Kim B.J. Hancock B.M. Bermudez A. Del Cid N. Reyes E. van Sorge N.M. Lauth X. Smurthwaite C.A. Hilton B.J. Stotland A. Bacterial induction of snail1 contributes to blood-brain barrier disruption J. Clin. Invest. 2015 125 2473 2483 10.1172/JCI74159 25961453 PMC4497739 · DOI · Paper page
- [121]Rose R. Hauser S. Stump-Guthier C. Weiss C. Rohde M. Kim K.S. Ishikawa H. Schroten H. Schwerk C. Adam R. Virulence factor-dependent basolateral invasion of choroid plexus epithelial cells by pathogenic Escherichia coli in vitro Fems Microbiol. Lett. 2018 365 10.1093/femsle/fny274 30476042 PMC7190931 · DOI
- [122]Kim K.S. Itabashi H. Gemski P. Sadoff J. Warren R.L. Cross A.S. The k1-capsule is the critical determinant in the development of escherichia-coli meningitis in the rat J. Clin. Invest. 1992 90 897 905 10.1172/JCI115965 1326000 PMC329944 · DOI
- [123]Cross A.S. Kim K.S. Wright D.C. Sadoff J.C. Gemski P. Role of lipopolysaccharide and capsule in the serum resistance of bacteremic strains of escherichia-coli J. Infect. Dis. 1986 154 497 503 10.1093/infdis/154.3.497 3525697 · DOI
- [124]Logue C.M. Doetkott C. Mangiamele P. Wannemuehler Y.M. Johnson T.J. Tivendale K.A. Li G.W. Sherwood J.S. Nolan L.K. Genotypic and phenotypic traits that distinguish neonatal meningitis-associated escherichia coli from fecal e. Coli isolates of healthy human hosts Appl. Environ. Microbiol. 2012 78 5824 5830 10.1128/AEM.07869-11 22706051 PMC3406136 · DOI
- [125]Teng C.H. Cai M. Shin S. Xie Y. Kim K.J. Khan N.A. Di Cello F. Kim K.S. Escherichia coli k1 rs218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state Infect. Immun. 2005 73 2923 2931 10.1128/IAI.73.5.2923-2931.2005 15845498 PMC1087349 · DOI
- [126]Khan N.A. Shin S. Chung J.W. Kim K.J. Elliott S. Wang Y. Kim K.S. Outer membrane protein a and cytotoxic necrotizing factor-1 use diverse signaling mechanisms for escherichia coli k1 invasion of human brain microvascular endothelial cells Microb. Pathog. 2003 35 35 42 10.1016/S0882-4010(03)00090-1 12860457 · DOI
- [127]Huang S.H. Wan Z.S. Chen Y.H. Jong A.Y. Kim K.S. Further characterization of escherichia coli brain microvascular endothelial cell invasion gene ibea by deletion, complementation, and protein expression J. Infect. Dis. 2001 183 1071 1078 10.1086/319290 11237832 · DOI
- [128]Wang M.H. Kim K.S. Cytotoxic necrotizing factor 1 contributes to escherichia coli meningitis Toxins 2013 5 2270 2280 10.3390/toxins5112270 24284829 PMC3847726 · DOI
- [129]Prasadarao N.V. Identification of escherichia coli outer membrane protein a receptor on human brain microvascular endothelial cells Infect. Immun. 2002 70 4556 4563 10.1128/IAI.70.8.4556-4563.2002 12117968 PMC128170 · DOI
- [130]Reddy M.A. Wass C.A. Kim K.S. Schlaepfer D.D. Prasadarao N.V. Involvement of focal adhesion kinase in escherichia coli invasion of human brain microvascular endothelial cells Infect. Immun. 2000 68 6423 6430 10.1128/IAI.68.11.6423-6430.2000 11035755 PMC97729 · DOI
- [131]Reddy M.A. Prasadarao N.V. Wass C.A. Kim K.S. Phosphatidylinositol 3-kinase activation and interaction with focal adhesion kinase in escherichia coli k1 invasion of human brain microvascular endothelial cells J. Biol. Chem. 2000 275 36769 36774 10.1074/jbc.M007382200 10973983 · DOI
- [132]Sukumaran S.K. McNamara G. Prasadarao N.V. Escherichia coli k-1 interaction with human brain micro-vascular endothelial cells triggers phospholipase c-gamma1 activation downstream of phosphatidylinositol 3-kinase J. Biol. Chem. 2003 278 45753 45762 10.1074/jbc.M307374200 12952950 · DOI
- [133]Selvaraj S.K. Periandythevar P. Prasadarao N.V. Outer membrane protein a of escherichia coli k1 selectively enhances the expression of intercellular adhesion molecule-1 in brain microvascular endothelial cells Microb. Infect. 2007 9 547 557 10.1016/j.micinf.2007.01.020 17368067 PMC1993839 · DOI
- [134]Prasadarao N.V. Wass C.A. Stins M.F. Shimada H. Kim K.S. Outer membrane protein a-promoted actin condensation of brain microvascular endothelial cells is required for escherichia coli invasion Infect. Immun. 1999 67 5775 5783 10531228 PMC96954
- [135]Sukumaran S.K. Quon M.J. Prasadarao N.V. Escherichia coli k1 internalization via caveolae requires caveolin-1 and protein kinase c alpha interaction in human brain microvascular endothelial cells J. Biol. Chem. 2002 277 50716 50724 10.1074/jbc.M208830200 12386163 · DOI
- [136]Kim K.J. Elliott S.J. Di Cello F. Stins M.F. Kim K.S. The k1 capsule modulates trafficking of e-coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells Cell. Microbiol. 2003 5 245 252 10.1046/j.1462-5822.2003.t01-1-00271.x 12675682 · DOI
- [137]Yang R.C. Huang F. Fu J.Y. Dou B.B. Xu B.J. Miao L. Liu W.T. Yang X.P. Tan C. Chen H.C. Differential transcription profiles of long non-coding rnas in primary human brain microvascular endothelial cells in response to meningitic escherichia coli Sci. Rep. 2016 6 38903 10.1038/srep38903 27958323 PMC5153642 · DOI
- [138]Yang R.C. Qu X.Y. Xiao S.Y. Li L. Xu B.J. Fu J.Y. Lv Y.J. Amjad N. Tan C. Kim K.S. Meningitic escherichia coli-induced upregulation of pdgf-b and icam-1 aggravates blood-brain barrier disruption and neuroinflammatory response J. Neuroinflamm. 2019 16 101 10.1186/s12974-019-1497-1 PMC6521501 31092253 · DOI
- [139]Sukumaran S.K. Prasadarao N.V. Escherichia coli k1 invasion increases human brain microvascular endothelial cell monolayer permeability by disassembling vascular-endothelial cadherins at tight junctions J. Infect. Dis. 2003 188 1295 1309 10.1086/379042 14593586 · DOI
- [140]Mittal R. Gonzalez-Gomez I. Goth K.A. Prasadarao N.V. Inhibition of inducible nitric oxide controls pathogen load and brain damage by enhancing phagocytosis of escherichia coli k1 in neonatal meningitis Am. J. Pathol. 2010 176 1292 1305 10.2353/ajpath.2010.090851 20093483 PMC2832150 · DOI
- [141]Shanmuganathan M.V. Krishnan S. Fu X.W. Prasadarao N.V. Attenuation of biopterin synthesis prevents escherichia coli k1 invasion of brain endothelial cells and the development of meningitis in newborn mice J. Infect. Dis. 2013 207 61 71 10.1093/infdis/jis656 23100563 PMC3523800 · DOI
- [142]Liu W.T. Lv Y.J. Yang R.C. Fu J.Y. Liu L. Wang H. Cao Q. Tan C. Chen H.C. Wang X.R. New insights into meningitic escherichia coli infection of brain microvascular endothelial cells from quantitative proteomics analysis J. Neuroinflamm. 2018 15 291 10.1186/s12974-018-1325-z 30340642 PMC6195690 · DOI
- [143]Zhang K. Shi M.J. Niu Z. Chen X. Wei J.Y. Miao Z.W. Zhao W.D. Chen Y.H. Activation of brain endothelium by escherichia coli k1 virulence factor cgld promotes polymorphonuclear leukocyte transendothelial migration Med. Microbiol. Immunol. 2019 208 59 68 10.1007/s00430-018-0560-3 30171337 · DOI
- [144]Coureuil M. Lecuyer H. Bourdoulous S. Nassif X. A journey into the brain: Insight into how bacterial pathogens cross blood-brain barriers Nat. Rev. Microbiol. 2017 15 149 159 10.1038/nrmicro.2016.178 28090076 · DOI
- [145]Schneider M.C. Exley R.M. Chan H. Feavers I. Kang Y.H. Sim R.B. Tang C.M. Functional significance of factor h binding to neisseria meningitidis J. Immunol. 2006 176 7566 7575 10.4049/jimmunol.176.12.7566 16751403 · DOI
- [146]Seib K.L. Scarselli M. Comanducci M. Toneatto D. Masignani V. Neisseria meningitidis factor h-binding protein fhbp: A key virulence factor and vaccine antigen Expert Rev. Vaccines 2015 14 841 859 10.1586/14760584.2015.1016915 25704037 · DOI
- [147]Kim B.J. Shusta E.V. Doran K.S. Past and current perspectives in modeling bacteria and blood brain barrier interactions Front. Microbiol. 2019 10 1336 10.3389/fmicb.2019.01336 31263460 PMC6585309 · DOI
- [148]Stephens D.S. Biology and pathogenesis of the evolutionarily successful, obligate human bacterium neisseria meningitidis Vaccine 2009 27 B71 B77 10.1016/j.vaccine.2009.04.070 19477055 PMC2712446 · DOI
- [149]Gomes S.F.M. Westermann A.J. Sauerwein T. Hertlein T. Forstner K.U. Ohlsen K. Metzger M. Shusta E.V. Kim B.J. Appelt-Menzel A. Induced pluripotent stem cell-derived brain endothelial cells as a cellular model to study neisseria meningitidis infection Front. Microbiol. 2019 10 10.3389/fmicb.2019.01181 PMC6548865 31191497 · DOI
- [150]Nagele V. Heesemann J. Schielke S. Jimenez-Soto L.F. Kurzai O. Ackermann N. Neisseria meningitidis adhesin nada targets beta1 integrins: Functional similarity to yersinia invasin J. Biol. Chem. 2011 286 20536 20546 10.1074/jbc.M110.188326 21471204 PMC3121457 · DOI
- [151]Pizza M. Rappuoli R. Neisseria meningitidis: Pathogenesis and immunity Curr. Opin. Microbiol. 2015 23 68 72 10.1016/j.mib.2014.11.006 25461575 · DOI
- [152]Unkmeir A. Latsch K. Dietrich G. Wintermeyer E. Schinke B. Schwender S. Kim K.S. Eigenthaler M. Frosch M. Fibronectin mediates opc-dependent internalization of neisseria meningitidis in human brain microvascular endothelial cells Mol. Microbiol. 2002 46 933 946 10.1046/j.1365-2958.2002.03222.x 12421301 · DOI
- [153]Deghmane A.E. Giorgini D. Larribe M. Alonso J.M. Taha M.K. Down-regulation of pili and capsule of neisseria meningitidis upon contact with epithelial cells is mediated by crga regulatory protein Mol. Microbiol. 2002 43 1555 1564 10.1046/j.1365-2958.2002.02838.x 11952904 · DOI
- [154]Berry J.L. Pelicic V. Exceptionally widespread nanomachines composed of type iv pilins: The prokaryotic swiss army knives Fems Microbiol. Rev. 2015 39 134 154 10.1093/femsre/fuu001 25793961 PMC4471445 · DOI
- [155]Bernard S.C. Simpson N. Join-Lambert O. Federici C. Laran-Chich M.P. Maissa N. Bouzinba-Segard H. Morand P.C. Chretien F. Taouji S. Pathogenic neisseria meningitidis utilizes cd147 for vascular colonization Nat. Med. 2014 20 725 731 10.1038/nm.3563 24880614 PMC7095922 · DOI
- [156]Rudel T. Scheurerpflug I. Meyer T.F. Neisseria pilc protein identified as type-4 pilus tip-located adhesin Nature 1995 373 357 359 10.1038/373357a0 7830772 · DOI
- [157]Nassif X. Beretti J.L. Lowy J. Stenberg P. O’Gaora P. Pfeifer J. Normark S. So M. Roles of pilin and pilc in adhesion of neisseria meningitidis to human epithelial and endothelial cells Proc. Natl. Acad. Sci. USA 1994 91 3769 3773 10.1073/pnas.91.9.3769 7909606 PMC43663 · DOI
- [158]Morand P.C. Tattevin P. Eugene E. Beretti J.L. Nassif X. The adhesive property of the type iv pilus-associated component pilc1 of pathogenic neisseria is supported by the conformational structure of the n-terminal part of the molecule Mol. Microbiol. 2001 40 846 856 10.1046/j.1365-2958.2001.02452.x 11401692 · DOI
- [159]Virji M. Pathogenic neisseriae: Surface modulation, pathogenesis and infection control Nat. Rev. Microbiol. 2009 7 274 286 10.1038/nrmicro2097 19287450 · DOI
- [160]Carbonnelle E. Hill D.J. Morand P. Griffiths N.J. Bourdoulous S. Murillo I. Nassif X. Virji M. Meningococcal interactions with the host Vaccine 2009 27 B78 B89 10.1016/j.vaccine.2009.04.069 19481311 · DOI
- [161]Virji M. Makepeace K. Ferguson D.J. Achtman M. Moxon E.R. Meningococcal opa and opc proteins: Their role in colonization and invasion of human epithelial and endothelial cells Mol. Microbiol. 1993 10 499 510 10.1111/j.1365-2958.1993.tb00922.x 7968528 · DOI
- [162]Gray-Owen S.D. Neisserial opa proteins: Impact on colonization, dissemination and immunity Scand. J. Infect. Dis. 2003 35 614 618 10.1080/00365540310016042 14620144 · DOI
- [163]Sa E.C.C. Griffiths N.J. Virji M. Neisseria meningitidis opc invasin binds to the sulphated tyrosines of activated vitronectin to attach to and invade human brain endothelial cells PLoS Pathog 2010 6 e1000911 20502634 PMC2873925
- [164]Simonis A. Hebling S. Gulbins E. Schneider-Schaulies S. Schubert-Unkmeir A. Differential activation of acid sphingomyelinase and ceramide release determines invasiveness of neisseria meningitidis into brain endothelial cells PLoS Path. 2014 10 e1004160 10.1371/journal.ppat.1004160 24945304 PMC4055770 · DOI
- [165]Metruccio M.M. Pigozzi E. Roncarati D. Berlanda Scorza F. Norais N. Hill S.A. Scarlato V. Delany I. A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements PLoS Pathog 2009 5 e1000710 10.1371/journal.ppat.1000710 20041170 PMC2791445 · DOI
- [166]Comanducci M. Bambini S. Caugant D.A. Mora M. Brunelli B. Capecchi B. Ciucchi L. Rappuoli R. Pizza M. Nada diversity and carriage in neisseria meningitidis Infect. Immun. 2004 72 4217 4223 10.1128/IAI.72.7.4217-4223.2004 15213166 PMC427459 · DOI
- [167]Capecchi B. Adu-Bobie J. Di Marcello F. Ciucchi L. Masignani V. Taddei A. Rappuoli R. Pizza M. Arico B. Neisseria meningitidis nada is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells Mol. Microbiol. 2005 55 687 698 10.1111/j.1365-2958.2004.04423.x 15660996 · DOI
- [168]Scietti L. Sampieri K. Pinzuti I. Bartolini E. Benucci B. Liguori A. Haag A.F. Lo Surdo P. Pansegrau W. Nardi-Dei V. Exploring host-pathogen interactions through genome wide protein microarray analysis Sci. Rep. 2016 6 27996 10.1038/srep27996 27302108 PMC4908583 · DOI
- [169]Simonis A. Schubert-Unkmeir A. Interactions of meningococcal virulence factors with endothelial cells at the human blood-cerebrospinal fluid barrier and their role in pathogenicity Febs Lett. 2016 590 3854 3867 10.1002/1873-3468.12344 27498906 · DOI
- [170]Lambotin M. Hoffmann I. Laran-Chich M.P. Nassif X. Couraud P.O. Bourdoulous S. Invasion of endothelial cells by neisseria meningitidis requires cortactin recruitment by a phosphoinositide-3-kinase/rac1 signalling pathway triggered by the lipo-oligosaccharide J. Cell Sci. 2005 118 3805 3816 10.1242/jcs.02514 16076899 · DOI
- [171]Soyer M. Charles-Orszag A. Lagache T. Machata S. Imhaus A.F. Dumont A. Millien C. Olivo-Marin J.C. Dumenil G. Early sequence of events triggered by the interaction of neisseria meningitidis with endothelial cells Cell. Microbiol. 2014 16 878 895 10.1111/cmi.12248 24320113 · DOI
- [172]Takahashi H. Watanabe H. Kim K.S. Yokoyama S. Yanagisawa T. The meningococcal cysteine transport system plays a crucial role in neisseria meningitidis survival in human brain microvascular endothelial cells Mbio 2018 9 10.1128/mBio.02332-18 30538184 PMC6299482 · DOI
- [173]Slanina H. Hebling S. Hauck C.R. Schubert-Unkmeir A. Cell invasion by neisseria meningitidis requires a functional interplay between the focal adhesion kinase, src and cortactin PLoS ONE 2012 7 e39613 10.1371/journal.pone.0039613 22768099 PMC3387252 · DOI
- [174]Schubert-Unkmeir A. Sokolova O. Panzner U. Eigenthaler M. Frosch M. Gene expression pattern in human brain endothelial cells in response to neisseria meningitidis Infect. Immun. 2007 75 899 914 10.1128/IAI.01508-06 17130252 PMC1828482 · DOI
- [175]Sa E.C.C. Griffiths N.J. Murillo I. Virji M. Neisseria meningitidis opc invasin binds to the cytoskeletal protein alpha-actinin Cell. Microbiol. 2009 11 389 405 10.1111/j.1462-5822.2008.01262.x 19016781 PMC2688670 · DOI
- [176]Coureuil M. Lecuyer H. Scott M.G.H. Boularan C. Enslen H. Soyer M. Mikaty G. Bourdoulous S. Nassif X. Marullo S. Meningococcus hijacks a beta 2-adrenoceptor/beta-arrestin pathway to cross brain microvasculature endothelium Cell 2010 143 1149 1160 10.1016/j.cell.2010.11.035 21183077 · DOI
- [177]Schubert-Unkmeir A. Konrad C. Slanina H. Czapek F. Hebling S. Frosch M. Neisseria meningitidis induces brain microvascular endothelial cell detachment from the matrix and cleavage of occludin: A role for mmp-8 PLoS Path. 2010 6 e1000874 10.1371/journal.ppat.1000874 PMC2861698 20442866 · DOI
- [178]Coureuil M. Mikaty G. Miller F. Lecuyer H. Bernard C. Bourdoulous S. Dumenil G. Mege R.M. Weksler B.B. Romero I.A. Meningococcal type iv pili recruit the polarity complex to cross the brain endothelium Science 2009 325 83 87 10.1126/science.1173196 19520910 PMC3980637 · DOI
- [179]Waage A. Brandtzaeg P. Halstensen A. Kierulf P. Espevik T. The complex pattern of cytokines in serum from patients with meningococcal septic shock-association between interleukin-6, interleukin-1, and fatal outcome J. Exp. Med. 1989 169 333 338 10.1084/jem.169.1.333 2783334 PMC2189201 · DOI
- [180]Sokolova O. Heppel N. Jagerhuber R. Kim K.S. Frosch M. Eigenthaler M. Schubert-Unkmeir A. Interaction of neisseria meningitidis with human brain microvascular endothelial cells: Role of map- and tyrosine kinases in invasion and inflammatory cytokine release Cell. Microbiol. 2004 6 1153 1166 10.1111/j.1462-5822.2004.00422.x 15527495 · DOI
- [182]Zarei A.E. Almehdar H.A. Redwan E.M. Hib vaccines: Past, present, and future perspectives J. Immunol. Res. 2016 10.1155/2016/7203587 26904695 PMC4745871 · DOI
- [183]Bakaletz L.O. Novotny L.A. Nontypeable haemophilus influenzae (nthi) Trends Microbiol. 2018 26 727 728 10.1016/j.tim.2018.05.001 29793827 · DOI
- [184]Doran K.S. Banerjee A. Disson O. Lecuit M. Concepts and mechanisms: Crossing host barriers Cold Spring Harb. Perspect. Med. 2013 3 a010090 10.1101/cshperspect.a010090 23818514 PMC3685877 · DOI
- [185]Van Ham S.M. van Alphen L. Mooi F.R. van Putten J.P. Phase variation of h. Influenzae fimbriae: Transcriptional control of two divergent genes through a variable combined promoter region Cell 1993 73 1187 1196 10.1016/0092-8674(93)90647-9 8513502 · DOI
- [186]Cundell D.R. Gerard N.P. Gerard C. Idanpaan-Heikkila I. Tuomanen E.I. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor Nature 1995 377 435 438 10.1038/377435a0 7566121 · DOI
- [187]Swords W.E. Ketterer M.R. Shao J. Campbell C.A. Weiser J.N. Apicella M.A. Binding of the non-typeable haemophilus influenzae lipooligosaccharide to the paf receptor initiates host cell signalling Cell. Microbiol. 2001 3 525 536 10.1046/j.1462-5822.2001.00132.x 11488814 · DOI
- [188]Radin J.N. Orihuela C.J. Murti G. Guglielmo C. Murray P.J. Tuomanen E.I. Beta-arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of streptococcus pneumoniae Infect. Immun. 2005 73 7827 7835 10.1128/IAI.73.12.7827-7835.2005 16299272 PMC1307033 · DOI
- [189]Caporarello N. Olivieri M. Cristaldi M. Scalia M. Toscano M.A. Genovese C. Addamo A. Salmeri M. Lupo G. Anfuso C.D. Blood-brain barrier in a haemophilus influenzae type a in vitro infection: Role of adenosine receptors a(2a) and a(2b) Mol. Neurobiol. 2018 55 5321 5336 10.1007/s12035-017-0769-y 28921456 · DOI
- [190]Wispelwey B. Lesse A.J. Hansen E.J. Scheld W.M. Haemophilus influenzae lipopolysaccharide-induced blood brain barrier permeability during experimental meningitis in the rat J. Clin. Invest. 1988 82 1339 1346 10.1172/JCI113736 3262627 PMC442689 · DOI
- [191]Wispelwey B. Hansen E.J. Scheld W.M. Haemophilus influenzae outer membrane vesicle-induced blood-brain barrier permeability during experimental meningitis Infect. Immun. 1989 57 2559 2562 2787292 PMC313486
- [192]Parisi D.N. Martinez L.R. Intracellular haemophilus influenzae invades the brain: Is zyxin a critical blood brain barrier component regulated by tnf-alpha? Virulence 2014 5 645 647 10.4161/viru.36086 25127527 PMC4139403 · DOI
- [193]Kostyanev T.S. Sechanova L.P. Virulence factors and mechanisms of antibiotic resistance of haemophilus influenzae Folia Med. 2012 54 19 23 10.2478/v10153-011-0073-y 22908826 · DOI
- [194]Yau B. Hunt N.H. Mitchell A.J. Too L.K. Bloodbrain barrier pathology and cns outcomes in streptococcus pneumoniae meningitis Int. J. Mol. Sci. 2018 19 3555 10.3390/ijms19113555 30423890 PMC6275034 · DOI
- [195]Ferrieri P. Burke B. Nelson J. Production of bacteremia and meningitis in infant rats with group-b streptococcal serotypes Infect. Immun. 1980 27 1023 1032 6991426 PMC550875
- [196]Nassif X. Bourdoulous S. Eugene E. Couraud P.O. How do extracellular pathogens cross the blood-brain barrier? Trends Microbiol. 2002 10 10.1016/S0966-842X(02)02349-1 11973156 · DOI
Cited by
Sorted by citations
Deng, L., Spencer, B. L., Holmes, J. A., Mu, R., Rego, S., Weston, T. A., Hu, Y., Sanches, G. F., Yoon, S., Park, N., et al. (2019) · PLOS Pathogens · doi:10.1371/journal.ppat.1007848 · Cited by 74 · see citing works
Patiño Patiño, J. J., Osorio-Rodríguez, E., García Toscano, Y. P., Filott Tamara, M., De-Ávila-Arias, M., Rodríguez Sanjuán, A., Villarreal-Camacho, J. L., Martínez De la Rosa, W., Bilbao Ramírez, J., Coronell-Rodríguez, W., et al. (2026) · Microbiology Spectrum · doi:10.1128/spectrum.02122-25
“The detection of enteroviral RNA in the CSF is therefore a direct indicator of CNS involvement (23–25).”
- Authors
- Herold, R., Schroten, H., & Schwerk, C.
- Affiliations
- Heidelberg University (DE)
- Corresponding author
- Schwerk, Christian
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2019-10-29
- Volume
- 20
- Issue
- 21
- Pages
- 5393
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC6862235
- OpenAlex
- W2982456408
- Cited by
- 48
- References
- 10
- Citations by year
- 2026: 1 · 2025: 10 · 2024: 9 · 2023: 9 · 2022: 5 · 2021: 7 · 2020: 5 · 2019: 2
- FWCI
- 0.69
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Deutsche Forschungsgemeinschaft
- Universität Heidelberg
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- meningitis, virulence factors, blood-brain barrier, blood-CSF barrier, bacterial adhesion, host cell invasion, intracellular survival, host cell signaling, inflammation, barrier function
- MeSH terms
- Animals, Blood-Brain Barrier, Brain, Central Nervous System, Cerebrospinal Fluid, Gram-Negative Bacteria, Gram-Positive Bacteria, Humans, Virulence, Signal Transduction, Meningitis, Bacterial, Virulence Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review