1,761
Views
8
CrossRef citations to date
0
Altmetric
Research paper

Bacteria elevate extracellular adenosine to exploit host signaling for blood-brain barrier disruption

, ORCID Icon, , , , , , , & show all
Pages 980-994 | Received 14 Apr 2020, Accepted 07 Jul 2020, Published online: 10 Aug 2020

References

  • McGill F, Heyderman RS, Panagiotou S, et al. Acute bacterial meningitis in adults. Lancet. 2016;388:3036–3047.
  • Zunt JR, Kassebaum NJ, Blake N, et al. Global, regional, and national burden of meningitis, 1990–2016: a systematic analysis for the global burden of disease study 2016. Lancet Neurol. 2018;17:1061–1082.
  • van de Beek D, Brouwer M, Hasbun R, et al. Community-acquired bacterial meningitis. Nat Rev Dis Primers. 2016;2:16074.
  • Coureuil M, Lecuyer H, Bourdoulous S, et al. A journey into the brain: insight into how bacterial pathogens cross blood-brain barriers. Nature Rev Microbiol. 2017;15:149–159.
  • Join-Lambert O, Morand PC, Carbonnelle E, et al. Mechanisms of meningeal invasion by a bacterial extracellular pathogen, the example of Neisseria meningitidis. Prog Neurobiol. 2010;91:130–139.
  • Dando SJ, Mackay-Sim A, Norton R, et al. Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev. 2014;27:691–726.
  • Kim KS. Mechanisms of microbial traversal of the blood-brain barrier. Nature Rev Microbiol. 2008;6:625–634.
  • Coureuil M, Mikaty G, Miller F, et al. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science. 2009;325:83–87.
  • Nikulin J, Panzner U, Frosch M, et al. Intracellular survival and replication of Neisseria meningitidis in human brain microvascular endothelial cells. Int J Med Microbiol. 2006;296:553–558.
  • Kim BJ, Hancock BM, Bermudez A, et al. Bacterial induction of Snail1 contributes to blood-brain barrier disruption. J Clin Invest. 2015;125:2473–2483.
  • Nizet V, Kim KS, Stins M, et al. Invasion of brain microvascular endothelial cells by group B streptococci. Infect Immun. 1997;65:5074–5081.
  • Cutting AS, Del Rosario Y, Mu R, et al. The role of autophagy during group B Streptococcus infection of blood-brain barrier endothelium. J Biol Chem. 2014;289:35711–35723.
  • Krishnan S, Fernandez GE, Sacks DB, et al. IQGAP1 mediates the disruption of adherens junctions to promote Escherichia coli K1 invasion of brain endothelial cells. Cell Microbiol. 2012;14:1415–1433.
  • Huang SH, Wass C, Fu Q, et al. Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect Immun. 1995;63:4470–4475.
  • Gao X, Qian J, Zheng S, et al. Overcoming the blood-brain barrier for delivering drugs into the brain by using adenosine receptor nanoagonist. ACS Nano. 2014;8:3678–3689.
  • Carman AJ, Mills JH, Krenz A, et al. Adenosine receptor signaling modulates permeability of the blood-brain barrier. J Neurosci. 2011;31:13272–13280.
  • Bynoe MS, Viret C, Yan A, et al. Adenosine receptor signaling: a key to opening the blood-brain door. Fluids Barriers CNS. 2015;12:20.
  • Kim DG, Bynoe MS. A2A adenosine receptor regulates the human blood-brain barrier permeability. Mol Neurobiol. 2015;52:664–678.
  • Mills JH, Alabanza L, Weksler BB, et al. Human brain endothelial cells are responsive to adenosine receptor activation. Purinergic Signal. 2011;7:265–273.
  • Mills JH, Thompson LF, Mueller C, et al. CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2008;105:9325–9330.
  • Segura M, Zheng H, de Greeff A, et al. Latest developments on Streptococcus suis: an emerging zoonotic pathogen: part 2. Future Microbiol. 2014;9:587–591.
  • Tang J, Wang C, Feng Y, et al. Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med. 2006;3:e151.
  • Liu P, Pian Y, Li X, et al. Streptococcus suis adenosine synthase functions as an effector in evasion of PMN-mediated innate immunity. J Infect Dis. 2014;210:35–45.
  • Thammavongsa V, Kern JW, Missiakas DM, et al. Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med. 2009;206:2417–2427.
  • Firon A, Dinis M, Raynal B, et al. Extracellular nucleotide catabolism by the group B Streptococcus ectonucleotidase NudP increases bacterial survival in blood. J Biol Chem. 2014;289:5479–5489.
  • Fan J, Zhang Y, Chuang-Smith ON, et al. Ecto-5ʹ-nucleotidase: a candidate virulence factor in Streptococcus sanguinis experimental endocarditis. PLoS One. 2012;7:e38059.
  • Strazza M, Maubert ME, Pirrone V, et al. Co-culture model consisting of human brain microvascular endothelial and peripheral blood mononuclear cells. J Neurosci Methods. 2016;269:39–45.
  • Dominguez-Punaro MC, Segura M, Plante MM, et al. Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol. 2007;179:1842–1854.
  • Kong D, Chen Z, Wang J, et al. Interaction of factor H-binding protein of Streptococcus suis with globotriaosylceramide promotes the development of meningitis. Virulence. 2017;8:1290–1302.
  • Chang YC, Wang Z, Flax LA, et al. Glycosaminoglycan binding facilitates entry of a bacterial pathogen into central nervous systems. PLoS Pathog. 2011;7:e1002082.
  • Chang YC, Olson J, Beasley FC, et al. Group B Streptococcus engages an inhibitory Siglec through sialic acid mimicry to blunt innate immune and inflammatory responses in vivo. PLoS Pathog. 2014;10:e1003846.
  • Doran KS, Liu GY, Nizet V. Group B streptococcal β-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. J Clin Investig. 2003;112:736–744.
  • Doran KS, Engelson EJ, Khosravi A, et al. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest. 2005;115:2499–2507.
  • Yang T, Gao X, Sandberg M, et al. Abrogation of adenosine A1 receptor signalling improves metabolic regulation in mice by modulating oxidative stress and inflammatory responses. Diabetologia. 2015;58:1610–1620.
  • Gorska AM, Golembiowska K. The role of adenosine A1 and A2A receptors in the caffeine effect on MDMA-induced DA and 5-HT release in the mouse striatum. Neurotox Res. 2015;27:229–245.
  • Synnestvedt K, Furuta GT, Comerford KM, et al. Ecto-5ʹ-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest. 2002;110:993–1002.
  • Shechter R, Miller O, Yovel G, et al. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity. 2013;38:555–569.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8:2281–2308.
  • Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11:783–784.
  • Mincham KT, Scott NM, Lauzon-Joset JF, et al. Transplacental immune modulation with a bacterial-derived agent protects against allergic airway inflammation. J Clin Invest. 2018;128:4856–4869.
  • Sato H, Silveira L, Spagnolo P, et al. CC chemokine receptor 5 gene polymorphisms in beryllium disease. Eur Respir J. 2010;36:331–338.
  • Fowler VG Jr., Das AF, Lipka-Diamond J, et al. Exebacase for patients with Staphylococcus aureus bloodstream infection and endocarditis. J Clin Invest. 2020;130:3750–3760.
  • Shi Y, Zhang L, Pu H, et al. Rapid endothelial cytoskeletal reorganization enables early blood-brain barrier disruption and long-term ischaemic reperfusion brain injury. Nat Commun. 2016;7:10523.
  • Eigenmann DE, Xue G, Kim KS, et al. Comparative study of four immortalized human brain capillary endothelial cell lines, hCMEC/D3, hBMEC, TY10, and BB19, and optimization of culture conditions, for an in vitro blood-brain barrier model for drug permeability studies. Fluids Barriers CNS. 2013;10:33.
  • Shi Y, Jiang X, Zhang L, et al. Endothelium-targeted overexpression of heat shock protein 27 ameliorates blood-brain barrier disruption after ischemic brain injury. Proc Natl Acad Sci U S A. 2017;114:E1243–E52.
  • Chen J, Luo Y, Hui H, et al. CD146 coordinates brain endothelial cell-pericyte communication for blood-brain barrier development. Proc Natl Acad Sci U S A. 2017;114:E7622–E31.
  • Charland N, Nizet V, Rubens CE, et al. Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells. Infect Immun. 2000;68:637–643.
  • Williams AE, Blakemore WF. Pathogenesis of meningitis caused by Streptococcus suis type 2. J Infect Dis. 1990;162:474–481.
  • Madsen LW, Svensmark B, Elvestad K, et al. Streptococcus suis serotype 2 infection in pigs: new diagnostic and pathogenetic aspects. J Comp Pathol. 2002;126:57–65.
  • Sanford SE. Gross and histopathological findings in unusual lesions caused by Streptococcus suis in pigs. I. Cardiac lesions. Can J Vet Res. 1987;51:481–485.
  • Tenenbaum T, Papandreou T, Gellrich D, et al. Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cell Microbiol. 2009;11:323–336.
  • Koshiba M, Kojima H, Huang S, et al. Memory of extracellular adenosine A2A purinergic receptor-mediated signaling in murine T cells. J Biol Chem. 1997;272:25881–25889.
  • Cronstein BN, Sitkovsky M. Adenosine and adenosine receptors in the pathogenesis and treatment of rheumatic diseases. Nat Rev Rheumatol. 2017;13:41–51.
  • Argaw AT, Gurfein BT, Zhang Y, et al. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci U S A. 2009;106:1977–1982.
  • Feoktistov I, Goldstein AE, Ryzhov S, et al. Differential expression of adenosine receptors in human endothelial cells: role of A2B receptors in angiogenic factor regulation. Circ Res. 2002;90:531–538.
  • Leibovich SJ, Chen JF, Pinhal-Enfield G, et al. Synergistic up-regulation of vascular endothelial growth factor expression in murine macrophages by adenosine A(2A) receptor agonists and endotoxin. Am J Pathol. 2002;160:2231–2244.
  • Ryzhov S, Novitskiy SV, Zaynagetdinov R, et al. Host A(2B) adenosine receptors promote carcinoma growth. Neoplasia. 2008;10:987–995.
  • Caporarello N, Olivieri M, Cristaldi M, et al. Blood-brain barrier in a haemophilus influenzae type a in vitro infection: role of adenosine receptors A2A and A2B. Mol Neurobiol. 2018;55:5321–5336.
  • Zagursky RJ, Ooi P, Jones KF, et al. Identification of a Haemophilus influenzae 5ʹ-nucleotidase protein: cloning of the nucA gene and immunogenicity and characterization of the NucA protein. Infect Immun. 2000;68:2525–2534.
  • Estrela AB, Turck P, Stutz E, et al. Release of periplasmic nucleotidase induced by human antimicrobial peptide in E. coli causes accumulation of the immunomodulator adenosine. PLoS One. 2015;10:e0138033.