Pericytes are protective in experimental pneumococcal meningitis through regulating leukocyte infiltration and blood–brain barrier function

Van de Beek D, Brouwer M, Hasbun R, Koedel U, Whitney CG, Wijdicks E. Community-acquired bacterial meningitis. Nat Rev Dis Primers. 2016;2:16074.

Article  PubMed  Google Scholar 

Van de Beek D, Brouwer MC, Koedel U, Wall EC. Community-acquired bacterial meningitis. Lancet. 2021;398:1171–83.

Article  PubMed  Google Scholar 

Weber JR, Tuomanen EI. Cellular damage in bacterial meningitis: an interplay of bacterial and host driven toxicity. J Neuroimmunol. 2007;184:45–52.

Article  CAS  PubMed  Google Scholar 

Zanluqui NG, McGavern DB. Bacterial meningitis hits an immunosuppressive nerve. Nature. 2023;615:396.

Article  CAS  PubMed  Google Scholar 

Pinho-Ribeiro FA, Deng L, Neel DV, Erdogan O, Basu H, Yang D, Choi S, Walker AJ, Carneiro-Nascimento S, He K, Wu G, Stevens B, Doran KS, Levy D, Chiu IM. Bacteria hijack a meningeal neuroimmune axis to facilitate brain invasion. Nature. 2023;615:472.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Polfliet MM, Zwijnenburg PJ, Van Furth AM, van Der P, Dopp EA, Renardel DL, van Kesteren-Hendrikx EM, Van Rooijen N, Dijkstra CD, van Den Berg TK. Meningeal and perivascular macrophages of the central nervous system play a protective role during bacterial meningitis. J Immunol. 2001;167:4644–50.

Article  CAS  PubMed  Google Scholar 

Trostdorf F, Bruck W, Schmitz-Salue M, Stuertz K, Hopkins SJ, van Rooijen N, Huitinga I, Nau R. Reduction of meningeal macrophages does not decrease migration of granulocytes into the CSF and brain parenchyma in experimental pneumococcal meningitis. J Neuroimmunol. 1999;99:205–10.

Article  CAS  PubMed  Google Scholar 

Händle P, Dyckhoff-Shen S, Angele B, Gorka O, Pfister H-W, Gross O, Kirschning CJ, Klein M, Koedel U. Macrophage pyroptosis aggravates inflammation and pathology in murine pneumococcal meningitis. ECCMID 2020, Paris (Online) ID5155: 2022.

Jansson D, Rustenhoven J, Feng S, Hurley D, Oldfield RL, Bergin PS, Mee EW, Faull RL, Dragunow M. A role for human brain pericytes in neuroinflammation. J Neuroinflammation. 2014;11:104.

Article  PubMed  PubMed Central  Google Scholar 

Rustenhoven J, Jansson D, Smyth LC, Dragunow M. Brain pericytes as mediators of neuroinflammation. Trends Pharmacol Sci. 2017;38:291–304.

Article  CAS  PubMed  Google Scholar 

Barkaway A, Attwell D, Korte N. Immune-vascular mural cell interactions: consequences for immune cell trafficking, cerebral blood flow, and the blood-brain barrier. Neurophotonics. 2022;9: 031914.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Medina-Flores F, Hurtado-Alvarado G, Deli MA, Gomez-Gonzalez B. The active role of pericytes during neuroinflammation in the adult brain. Cell Mol Neurobiol. 2022;43:525.

Article  PubMed  Google Scholar 

Alarcon-Martinez L, Yemisci M, Dalkara T. Pericyte morphology and function. Histol Histopathol. 2021;36:633–43.

CAS  PubMed  Google Scholar 

Nyul-Toth A, Kozma M, Nagyoszi P, Nagy K, Fazakas C, Hasko J, Molnar K, Farkas AE, Vegh AG, Varo G, Galajda P, Wilhelm I, Krizbai IA. Expression of pattern recognition receptors and activation of the non-canonical inflammasome pathway in brain pericytes. Brain Behav Immun. 2017;64:220–31.

Article  CAS  PubMed  Google Scholar 

Kovac A, Erickson MA, Banks WA. Brain microvascular pericytes are immunoactive in culture: cytokine, chemokine, nitric oxide, and LRP-1 expression in response to lipopolysaccharide. J Neuroinflammation. 2011;8:139.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pieper C, Marek JJ, Unterberg M, Schwerdtle T, Galla HJ. Brain capillary pericytes contribute to the immune defense in response to cytokines or LPS in vitro. Brain Res. 2014;1550:1–8.

Article  CAS  PubMed  Google Scholar 

Matsumoto J, Takata F, Machida T, Takahashi H, Soejima Y, Funakoshi M, Futagami K, Yamauchi A, Dohgu S, Kataoka Y. Tumor necrosis factor-alpha-stimulated brain pericytes possess a unique cytokine and chemokine release profile and enhance microglial activation. Neurosci Lett. 2014;578:133–8.

Article  CAS  PubMed  Google Scholar 

Pieper C, Pieloch P, Galla HJ. Pericytes support neutrophil transmigration via interleukin-8 across a porcine co-culture model of the blood-brain barrier. Brain Res. 2013;1524:1–11.

Article  CAS  PubMed  Google Scholar 

Kristensson K, Olsson Y. Accumulation of protein tracers in pericytes of the central nervous system following systemic injection in immature mice. Acta Neurol Scand. 1973;49:189–94.

Article  CAS  PubMed  Google Scholar 

Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557–61.

Article  CAS  PubMed  Google Scholar 

Villasenor R, Kuennecke B, Ozmen L, Ammann M, Kugler C, Gruninger F, Loetscher H, Freskgard PO, Collin L. Region-specific permeability of the blood-brain barrier upon pericyte loss. J Cereb Blood Flow Metab. 2017;37:3683–94.

Article  PubMed  PubMed Central  Google Scholar 

Mäe MA, He L, Nordling S, Vazquez-Liebanas E, Nahar K, Jung B, Li X, Tan BC, Foo JC, Cazenave GA, Wenk M, Zarb Y, Lavina B, Quaggin SE, Jeansson M, Gu C, Silver D, Michael VM, Butcher EC, Keller A, Betsholtz C. Single-cell analysis of blood-brain barrier response to pericyte loss. Circ Res. 2021;128(4):e46–62.

Article  PubMed  Google Scholar 

Caporarello N, Olivieri M, Cristaldi M, Scalia M, Toscano MA, Genovese C, Addamo A, Salmeri M, Lupo G, Anfuso CD. Blood-brain barrier in a haemophilus influenzae type a in vitro infection: role of adenosine receptors A2A and A2B. Mol Neurobiol. 2018;55(6):5321–36.

Article  CAS  PubMed  Google Scholar 

Salmeri M, Motta C, Anfuso CD, Amodeo A, Scalia M, Toscano MA, Alberghina M, Lupo G. VEGF receptor-1 involvement in pericyte loss induced by Escherichia coli in an in vitro model of blood brain barrier. Cell Microbiol. 2013;15:1367–84.

Article  CAS  PubMed  Google Scholar 

Gil E, Venturini C, Stirling D, Turner C, Tezera LB, Ercoli G, Baker T, Best K, Brown JS, Noursadeghi M. Pericyte derived chemokines amplify neutrophil recruitment across the cerebrovascular endothelial barrier. Front Immunol. 2022;13: 935798.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tigges U, Welser-Alves JV, Boroujerdi A, Milner R. A novel and simple method for culturing pericytes from mouse brain. Microvasc Res. 2012;84:74–80.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Martens P, Worm SW, Lundgren B, Konradsen HB, Benfield T. Serotype-specific mortality from invasive Streptococcus pneumoniae disease revisited. BMC Infect Dis. 2004;4:21.

Article  PubMed  PubMed Central  Google Scholar 

Müller A, Salmen A, Aebi S, de Gouveia L, von Gottberg A, Hathaway LJ. Pneumococcal serotype determines growth and capsule size in human cerebrospinal fluid. BMC Microbiol. 2020;20:16.

Article  PubMed  PubMed Central  Google Scholar 

Hathaway LJ, Grandgirard D, Valente LG, Tauber MG, Leib SL. Streptococcus pneumoniae capsule determines disease severity in experimental pneumococcal meningitis. Open Biol. 2016;6(3): 150269.

Article  PubMed  PubMed Central  Google Scholar 

Jim KK, Engelen-Lee J, van der Sar AM, Bitter W, Brouwer MC, Van der Ende A, Veening JW, Van de Beek D, Vandenbroucke-Grauls CM. Infection of zebrafish embryos with live fluorescent Streptococcus pneumoniae as a real-time pneumococcal meningitis model. J Neuroinflammation. 2016;13:188.

Article  PubMed  PubMed Central  Google Scholar 

Jim KK, Aprianto R, Koning R, Domenech A, Kurushima J, Van de Beek D, Vandenbroucke-Grauls CMJE, Bitter W, Veening JW. Pneumolysin promotes host cell necroptosis and bacterial competence during pneumococcal meningitis as shown by whole-animal dual RNA-seq. Cell Rep. 2022;41: 111851.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Renshaw SA, Loynes CA, Trushell DM, Elworthy S, Ingham PW, Whyte MK. A transgenic zebrafish model of neutrophilic inflammation. Blood. 2006;108:3976–8.

Article  CAS  PubMed  Google Scholar 

Benard EL, van der Sar AM, Ellett F, Lieschke GJ, Spaink HP, Meijer AH. Infection of zebrafish embryos with intracellular bacterial pathogens. J Vis Exp. 2012;15(61):3781.

Google Scholar 

Ando K, Fukuhara S, Izumi N, Nakajima H, Fukui H, Kelsh RN, Mochizuki N. Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish. Development. 2016;143:1328–39.

CAS  PubMed  PubMed Central  Google Scholar 

Malipiero U, Koedel U, Pfister HW, Leveen P, Bürki K, Reith W, Fontana A. TGF receptor II gene deletion in leukocytes prevents cerebral vasculitis in bacterial meningitis. Brain. 2006;129:2404–15.

Article  PubMed  Google Scholar 

Woehrl B, Brouwer MC, Murr C, Heckenberg SG, Baas F, Pfister HW, Zwinderman AH, Morgan BP, Barnum SR, van der Ende A, Koedel U. Complement component 5 contributes to poor disease outcome in humans and mice with pneumococcal meningitis. J Clin Invest. 2011;121:3943–53.

Article  CAS 

Comments (0)

No login
gif