Astrocytic tissue remodeling by the meningitis neurotoxin pneumolysin facilitates pathogen tissue penetration and produces interstitial brain edema

GLIA

Volumn 60, Issue 1, 2012, Pages 137-146

  Hupp, Sabrina ^a   Heimeroth, Vera ^a   Wippel, Carolin ^a   Förtsch, Christina ^a   Ma, Jiangtao ^b   Mitchell, Timothy J ^b   Iliev, Asparouh I ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Actin; Astrocyte; Cholesterol dependent cytolysin; Edema; Meningitis; Pneumolysin

Indexed keywords

PNEUMOLYSIN;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN; BRAIN EDEMA; ENDOCYTOSIS; FLUID RETENTION; MACROMOLECULE; MENINGITIS; MOUSE; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BACTERIAL PROTEINS; BRAIN; BRAIN EDEMA; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; EXTRACELLULAR FLUID; L-LACTATE DEHYDROGENASE; MENINGITIS; MICE; MICE, INBRED C57BL; NEUROTOXINS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS; TUBULIN;

EID: 81155148918     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21256     Document Type: Article

References (63)

1. Aktories K, Barbieri JT. 2005. Bacterial cytotoxins: Targeting eukaryotic switches. Nat Rev Microbiol 3: 397-410.
2. Alouf JE. 2000. Cholesterol-binding cytolytic protein toxins. Int J Med Microbiol 290: 351-356.
3. Annadurai D, Kasinathan R, Lyla PS. 2007. Acute toxicity effect of the venom of the marine snail, Conus zeylanicus. J Environ Biol 28: 825-828.
4. Barbuddhe SB, Chakraborty T. 2009. Listeria as an enteroinvasive gastrointestinal pathogen. Curr Top Microbiol Immunol 337: 173-195.
5. Barrias ES, Reignault LC, De Souza W, Carvalho TM. 2010. Dynasore, a dynamin inhibitor, inhibits Trypanosoma cruzi entry into peritoneal macrophages. PLoS ONE 5: e7764.
6. Binder DK, Papadopoulos MC, Haggie PM, Verkman AS. 2004. In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J Neurosci 24: 8049-8056.
7. Bosco A, Cusato K, Nicchia GP, Frigeri A, Spray DC. 2005. A developmental switch in the expression of aquaporin-4 and Kir4.1 from horizontal to müller cells in mouse retina. Invest Ophthalmol Vis Sci 46: 3869-3875.
8. Braun JS, Sublett JE, Freyer D, Mitchell TJ, Cleveland JL, Tuomanen EI, Weber JR. 2002. Pneumococcal pneumolysin and H(2)O(2) mediate brain cell apoptosis during meningitis. J Clin Invest 109: 19-27.
9. Canvin JR, Marvin AP, Sivakumaran M, Paton JC, Boulnois GJ, Andrew PW, Mitchell TJ. 1995. The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. J Infect Dis 172: 119-123.
10. Cockeran R, Anderson R, Feldman C. 2003. Pneumolysin in the immunopathogenesis and treatment of pneumococcal disease. Expert Rev Anti Infect Ther 1: 231-239.
11. Feltis BA, Kim AS, Kinneberg KM, Lyerly DL, Wilkins TD, Erlandsen SL, Wells CL. 1999. Clostridium difficile toxins may augment bacterial penetration of intestinal epithelium. Arch Surg 134: 1235-1241; discussion 1241-1242.
12. Ferrieri P, Burke B, Nelson J. 1980. Production of bacteremia and meningitis in infant rats with group B streptococcal serotypes. Infect Immun 27: 1023-1032.
13. Finnie JW. 1984. Histopathological changes in the brain of mice given Clostridium perfringens type D epsilon toxin. J Comp Pathol 94: 363-370.
14. Finnie JW, Manavis J, Blumbergs PC. 2008. Aquaporin-4 in acute cerebral edema produced by Clostridium perfringens type D epsilon toxin. Vet Pathol 45: 307-309.
15. Förtsch C, Hupp S, Ma J, Mitchell TJ, Maier E, Benz R, Iliev AI. 2011. Changes in astrocyte shape induced by sublytic concentrations of the cholesterol-dependent cytolysin pneumolysin still require pore-forming capacity. Toxins 3: 43-62.
16. Fujii J, Kinoshita Y, Matsukawa A, Villanueva SY, Yutsudo T, Yoshida S. 2009. Successful steroid pulse therapy for brain lesion caused by Shiga toxin 2 in rabbits. Microb Pathog 46: 179-184.
17. Gardenfors A, Nilsson F, Skagerberg G, Ungerstedt U, Nordstrom CH. 2002. Cerebral physiological and biochemical changes during vasogenic brain oedema induced by intrathecal injection of bacterial lipopolysaccharides in piglets. Acta Neurochir (Wien) 144: 601-608; discussion608-609.
18. Ghabriel MN, Zhu C, Reilly PL, Blumbergs PC, Manavis J, Finnie JW. 2000. Toxin-induced vasogenic cerebral oedema in a rat model. Acta Neurochir Suppl 76: 231-236.
19. Gunnarson E, Zelenina M, Axehult G, Song Y, Bondar A, Krieger P, Brismar H, Zelenin S, Aperia A. 2008. Identification of a molecular target for glutamate regulation of astrocyte water permeability. Glia 56: 587-596.
20. Hirst RA, Gosai B, Rutman A, Guerin CJ, Nicotera P, Andrew PW, O'Callaghan C. 2008. Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis. J Infect Dis 197: 744-751.
21. Hofman P, Le Negrate G, Mograbi B, Hofman V, Brest P, Alliana-Schmid A, Flatau G, Boquet P, Rossi B. 2000. Escherichia coli cytotoxic necrotizing factor-1 (CNF-1) increases the adherence to epithelia and the oxidative burst of human polymorphonuclear leukocytes but decreases bacteria phagocytosis. J Leukoc Biol 68: 522-528.
22. Holmin S, Mathiesen T. 2000. Intracerebral administration of interleukin-1beta and induction of inflammation, apoptosis, and vasogenic edema. J Neurosurg 92: 108-120.
23. Iliev AI, Djannatian JR, Nau R, Mitchell TJ, Wouters FS. 2007. Cholesterol-dependent actin remodeling via RhoA and Rac1 activation by the Streptococcus pneumoniae toxin pneumolysin. Proc Natl Acad Sci U S A 104: 2897-2902.
24. Iliev AI, Djannatian JR, Opazo F, Gerber J, Nau R, Mitchell TJ, Wouters FS. 2009. Rapid microtubule bundling and stabilization by the Streptococcus pneumoniae neurotoxin pneumolysin in a cholesterol-dependent, non-lytic and Src-kinase dependent manner inhibits intracellular trafficking. Mol Microbiol 71: 461-477.
25. Iliev AI, Stringaris AK, Nau R, Neumann H. 2004. Neuronal injury mediated via stimulation of microglial toll-like receptor-9 (TLR9). Faseb J 18: 412-414.
26. Imer M, Omay B, Uzunkol A, Erdem T, Sabanci P, Karasu A, Albayrak S, Sencer A, Hepgul K, Kaya M. 2009. Effect of magnesium, MK-801 and combination of magnesium and MK-801 on blood-brain barrier permeability and brain edema after experimental traumatic diffuse brain injury. Neurol Res 31: 977-981.
27. Jadhav V, Yamaguchi M, Obenaus A, Zhang JH. 2008. Matrix metalloproteinase inhibition attenuates brain edema after surgical brain injury. Acta Neurochir Suppl 102: 357-361.
28. Kastenbauer S, Pfister HW. 2003. Pneumococcal meningitis in adults: Spectrum of complications and prognostic factors in a series of 87 cases. Brain 126(Pt 5): 1015-1025.
29. Khan NA, Wang Y, Kim KJ, Chung JW, Wass CA, Kim KS. 2002. Cytotoxic necrotizing factor-1 contributes to Escherichia coli K1 invasion of the central nervous system. Journal Biol Chem 277: 15607-15612.
30. Koedel U, Scheld WM, Pfister HW. 2002. Pathogenesis and pathophysiology of pneumococcal meningitis. Lancet Infect Dis 2: 721-736.
31. Korchev YE, Bashford CL, Pasternak CA. 1992. Differential sensitivity of pneumolysin-induced channels to gating by divalent cations. J Membr Biol 127: 195-203.
32. Korchev YE, Bashford CL, Pederzolli C, Pasternak CA, Morgan PJ, Andrew PW, Mitchell TJ. 1998. A conserved tryptophan in pneumolysin is a determinant of the characteristics of channels formed by pneumolysin in cells and planar lipid bilayers. Biochem J 329(Pt 3): 571-577.
33. Lang AE, Schmidt G, Schlosser A, Hey TD, Larrinua IM, Sheets JJ, Mannherz HG, Aktories K. 2010. Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 327: 1139-1142.
34. Li W, Dai S, An J, Xiong R, Li P, Chen X, Zhao Y, Liu P, Wang H, Zhu P, Chen J, Zhou, Y. 2009. Genetic inactivation of adenosine A2A receptors attenuates acute traumatic brain injury in the mouse cortical impact model. Exp Neurol 215: 69-76.
35. Liu X, Han Q, Sun R, Li Z. 2008. Dexamethasone regulation of matrix metalloproteinase expression in experimental pneumococcal meningitis. Brain Res 1207: 237-243.
36. Lotz M, Ebert S, Esselmann H, Iliev AI, Prinz M, Wiazewicz N, Wiltfang J, Gerber J, Nau R. 2005. Amyloid beta peptide 1-40 enhances the action of Toll-like receptor-2 and -4 agonists but antagonizes Toll-like receptor-9-induced inflammation in primary mouse microglial cell cultures. J Neurochem 94: 289-298.
37. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, Thompson CM, Kurt-Jones E, Paton JC, Wessels MR, Golenbock DT. 2003. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A 100: 1966-1971.
38. Mitchell TJ, Walker JA, Saunders FK, Andrew PW, Boulnois GJ. 1989. Expression of the pneumolysin gene in Escherichia coli: Rapid purification and biological properties. Biochim Biophys Acta 1007: 67-72.
39. Nagaraja TN, Patel P, Gorski M, Gorevic PD, Patlak CS, Fenstermacher JD. 2005. In normal rat, intraventricularly administered insulin-like growth factor-1 is rapidly cleared from CSF with limited distribution into brain. Cerebrospinal Fluid Res 2: 5.
40. Nau R, Bruck W. 2002. Neuronal injury in bacterial meningitis: Mechanisms and implications for therapy. Trends Neurosci 25: 38-45.
41. Nicchia GP, Srinivas M, Li W, Brosnan CF, Frigeri A, Spray DC. 2005. New possible roles for aquaporin-4 in astrocytes: Cell cytoskeleton and functional relationship with connexin43. FASEB J 19: 1674-1676.
42. Papadopoulos MC, Binder DK, Verkman AS. 2005. Enhanced macromolecular diffusion in brain extracellular space in mouse models of vasogenic edema measured by cortical surface photobleaching. FASEB J 19: 425-427.
43. Papadopoulos MC, Verkman AS. 2005. Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J Biol Chem 280: 13906-13912.
44. Papadopoulos MC, Verkman AS. 2007. Aquaporin-4 and brain edema. Pediatr Nephrol 22: 778-784.
45. Pardridge W. 2011. Drug transport in brain via the cerebrospinal fluid. Fluids Barriers CNS 8: 7.
46. Pfister HW, Feiden W, Einhaupl KM. 1993. Spectrum of complications during bacterial meningitis in adults. Results of a prospective clinical study. Arch Neurol 50: 575-581.
47. Reiß A, Braun JS, Jäger K, Freyer D, Laube G, Bührer C, Felderhoff-Müser U, Stadelmann C, Nizet V, Weber JR. 2011. Bacterial pore-forming cytolysins induce neuronal damage in a rat model of neonatal meningitis. J Infect Dis 203: 393-400.
48. Richardson SE, Rotman TA, Jay V, Smith CR, Becker LE, Petric M, Olivieri NF, Karmali MA. 1992. Experimental verocytotoxemia in rabbits. Infect Immun 60: 4154-4167.
49. Sanz JM, Di Virgilio F. 2000. Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells. J Immunol 164: 4893-4898.
50. Solenov E, Watanabe H, Manley GT, Verkman AS. 2004. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286: C426-C432.
51. Spreer A, Kerstan H, Bottcher T, Gerber J, Siemer A, Zysk G, Mitchell TJ, Eiffert H, Nau R. 2003. Reduced release of pneumolysin by Streptococcus pneumoniae in vitro and in vivo after treatment with nonbacteriolytic antibiotics in comparison to ceftriaxone. Antimicrob Agents Chemother 47: 2649-2654.
52. Tanimura Y, Hiroaki Y, Fujiyoshi Y. 2009. Acetazolamide reversibly inhibits water conduction by aquaporin-4. J Struct Biol 166: 16-21.
53. Tauber MG, Shibl AM, Hackbarth CJ, Larrick JW, Sande MA. 1987. Antibiotic therapy, endotoxin concentration in cerebrospinal fluid, and brain edema in experimental Escherichia coli meningitis in rabbits. J Infect Dis 156: 456-462.
54. Tengvar C, Forssen M, Hultstrom D, Olsson Y, Pertoft H, Pettersson A. 1982. Measurement of edema in the nervous system. Use of Percoll density gradients for determination of specific gravity in cerebral cortex and white matter under normal conditions and in experimental cytotoxic brain edema. Acta Neuropathol 57: 143-150.
55. Tominaga S, Watanabe A, Tsuji T. 1991. Synergistic effect of bile acid, endotoxin, and ammonia on brain edema. Metab Brain Dis 6: 93-105.
56. Unterberg AW, Stover J, Kress B, Kiening KL. 2004. Edema and brain trauma. Neuroscience 129: 1021-1029.
57. Verkman AS, Binder DK, Bloch O, Auguste K, Papadopoulos MC. 2006. Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochim Biophys Acta 1758: 1085-1093.
58. Wellmer A, Zysk G, Gerber J, Kunst T, Von Mering M, Bunkowski S, Eiffert H, Nau R. 2002. Decreased virulence of a pneumolysin-deficient strain of Streptococcus pneumoniae in murine meningitis. Infect Immun 70: 6504-6508.
59. Werth JL, Park TS, Silbergeld DL, Rothman SM. 1998. Excitotoxic swelling occurs in oxygen and glucose deprived human cortical slices. Brain Res 782: 248-254.
60. Witzenrath M, Gutbier B, Hocke AC, Schmeck B, Hippenstiel S, Berger K, Mitchell TJ, de los Toyos JR, Rosseau S, Suttorp N, Schutte H. 2006. Role of pneumolysin for the development of acute lung injury in pneumococcal pneumonia. Crit Care Med 34: 1947-1954.
61. Yool AJ. 2007. Aquaporins: Multiple roles in the central nervous system. Neuroscientist 13: 470-485.
62. Zheng W, Watts LT, Holstein DM, Prajapati SI, Keller C, Grass EH, Walter CA, Lechleiter JD. 2010. Purinergic receptor stimulation reduces cytotoxic edema and brain infarcts in mouse induced by photothrombosis by energizing glial mitochondria. PLoS ONE 5: e14401.
63. Zysk G, Schneider-Wald BK, Hwang JH, Bejo L, Kim KS, Mitchell TJ, Hakenbeck R, Heinz HP. 2001. Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by Streptococcus pneumoniae. Infect Immun 69: 845-852.