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Published in: Journal of Neuroinflammation 1/2015

Open Access 01-12-2015 | Research

Vitamin D deficiency decreases survival of bacterial meningoencephalitis in mice

Authors: Marija Djukic, Nadine Sostmann, Thomas Bertsch, Marianne Mecke, Stefan Nessler, Anja Manig, Uwe-Karsten Hanisch, Jakob Triebel, L Cornelius Bollheimer, Cornel Sieber, Roland Nau

Published in: Journal of Neuroinflammation | Issue 1/2015

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Abstract

Background

Meningoencephalitis caused by Escherichia coli is associated with high rates of mortality and risk of neurological sequelae in newborns and infants and in older or immunocompromised adults. A high prevalence of neurological disorders has been observed in geriatric populations at risk of hypovitaminosis D.

Methods

In vivo, we studied the effects of vitamin D3 on survival and the host’s immune response in experimental bacterial meningoencephalitis in mice after intracerebral E. coli infection. To produce different systemic vitamin D3 concentrations, mice received a low, standard, or high dietary vitamin D3 supplementation. Bacterial titers in blood, spleen, and brain homogenates were determined. Leukocyte infiltration was assessed by histological scores, and tissue cytokine or chemokine concentrations were measured.

Results

Mice fed a diet with low vitamin D3 concentration died earlier than control animals after intracerebral infection. Vitamin D deficiency did not inhibit leukocyte recruitment into the subarachnoid space and did not lead to an increased density of bacteria in blood, spleen, or brain homogenates. The release of proinflammatory interleukin (IL)-6 was decreased and the release of anti-inflammatory IL-10 was increased in mice fed a diet with high vitamin D3 supplementation.

Conclusion

Our observations suggest a detrimental role of vitamin D deficiency in bacterial central nervous system infections. Vitamin D may exert immune regulatory functions.
Literature
1.
go back to reference Russo TA, Johnson JR: Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli : ExPEC. J Infect Dis 2000, 181:1753–1754.CrossRefPubMed Russo TA, Johnson JR: Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli : ExPEC. J Infect Dis 2000, 181:1753–1754.CrossRefPubMed
2.
go back to reference Silver RP, Aaronson W, Vann WF: The K1 capsular polysaccharide of Escherichia coli . Rev Infect Dis 1988, 10(Suppl. 2):S282–S286.CrossRefPubMed Silver RP, Aaronson W, Vann WF: The K1 capsular polysaccharide of Escherichia coli . Rev Infect Dis 1988, 10(Suppl. 2):S282–S286.CrossRefPubMed
3.
go back to reference Xie Y, Kim KJ, Kim KS: Current concepts on Escherichia coli K1 translocation of the blood–brain barrier. FEMS Immunol Med Microbiol 2004, 42:271–279.CrossRefPubMed Xie Y, Kim KJ, Kim KS: Current concepts on Escherichia coli K1 translocation of the blood–brain barrier. FEMS Immunol Med Microbiol 2004, 42:271–279.CrossRefPubMed
4.
go back to reference Kim KS, Itabashi H, Gemski P, Sadoff J, Warren RL, Cross AS: The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. J Clin Invest 1992, 90:897–905.PubMedCentralCrossRefPubMed Kim KS, Itabashi H, Gemski P, Sadoff J, Warren RL, Cross AS: The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. J Clin Invest 1992, 90:897–905.PubMedCentralCrossRefPubMed
5.
go back to reference Dietzman DE, Fischer GW, Schoenknecht FD: Neonatal Escherichia coli septicemia - bacterial counts in blood. J Pediatr 1974, 85:128–130.CrossRefPubMed Dietzman DE, Fischer GW, Schoenknecht FD: Neonatal Escherichia coli septicemia - bacterial counts in blood. J Pediatr 1974, 85:128–130.CrossRefPubMed
6.
go back to reference Briongos-Figuero LS, Morchón-Simón D, Aparicio-Blanco M, Garea García-Malvar MJ: Spontaneous meningitis due to Escherichia coli in the adult: a case report. Rev Clin Esp 2008, 208:262.CrossRefPubMed Briongos-Figuero LS, Morchón-Simón D, Aparicio-Blanco M, Garea García-Malvar MJ: Spontaneous meningitis due to Escherichia coli in the adult: a case report. Rev Clin Esp 2008, 208:262.CrossRefPubMed
7.
go back to reference Pitt J: K-1 antigen of Escherichia coli : epidemiology and serum sensitivity of pathogenic strains. Infect Immun 1978, 22:219–224.PubMedCentralPubMed Pitt J: K-1 antigen of Escherichia coli : epidemiology and serum sensitivity of pathogenic strains. Infect Immun 1978, 22:219–224.PubMedCentralPubMed
8.
go back to reference Kim KS: Strategy of Escherichia coli for crossing the blood–brain barrier. J Infect Dis 2002, 186(Suppl 2):220–224.CrossRef Kim KS: Strategy of Escherichia coli for crossing the blood–brain barrier. J Infect Dis 2002, 186(Suppl 2):220–224.CrossRef
9.
go back to reference Pouillot F, Chomton M, Blois H, Courroux C, Noelig J, Bidet P, Bingen E, Bonacorsi S: Efficacy of bacteriophage therapy in experimental sepsis and meningitis caused by a clone O25b:H4-ST131 Escherichia coli strain producing CTX-M-15. Antimicrob Agents Chemother 2012, 56:3568–3575.PubMedCentralCrossRefPubMed Pouillot F, Chomton M, Blois H, Courroux C, Noelig J, Bidet P, Bingen E, Bonacorsi S: Efficacy of bacteriophage therapy in experimental sepsis and meningitis caused by a clone O25b:H4-ST131 Escherichia coli strain producing CTX-M-15. Antimicrob Agents Chemother 2012, 56:3568–3575.PubMedCentralCrossRefPubMed
10.
11.
go back to reference van Duijn PJ, Dautzenberg MJ, Oostdijk EA: Recent trends in antibiotic resistance in European ICUs. Curr Opin Crit Care 2011, 17:658–665.CrossRefPubMed van Duijn PJ, Dautzenberg MJ, Oostdijk EA: Recent trends in antibiotic resistance in European ICUs. Curr Opin Crit Care 2011, 17:658–665.CrossRefPubMed
12.
go back to reference Schwalfenberg GK: A review of the critical role of vitamin D in the functioning of the immune system and the clinical implications of vitamin D deficiency. Mol Nutr Food Res 2011, 55:96–108.CrossRefPubMed Schwalfenberg GK: A review of the critical role of vitamin D in the functioning of the immune system and the clinical implications of vitamin D deficiency. Mol Nutr Food Res 2011, 55:96–108.CrossRefPubMed
16.
go back to reference Bikle DD: Vitamin D and the immune system: role in protection against bacterial infection. Curr Opin Nephrol Hypertens 2008, 17:348–352.CrossRefPubMed Bikle DD: Vitamin D and the immune system: role in protection against bacterial infection. Curr Opin Nephrol Hypertens 2008, 17:348–352.CrossRefPubMed
17.
go back to reference Rook GA, Steele J, Fraher L, Barker S, Karmali R, O'Riordan J, Stanford J: Vitamin D3, gamma interferon, and control of proliferation of Mycobacterium tuberculosis by human monocytes. Immunology 1986, 57:159–163.PubMedCentralPubMed Rook GA, Steele J, Fraher L, Barker S, Karmali R, O'Riordan J, Stanford J: Vitamin D3, gamma interferon, and control of proliferation of Mycobacterium tuberculosis by human monocytes. Immunology 1986, 57:159–163.PubMedCentralPubMed
18.
go back to reference Khoo AL, Chai L, Koenen H, Joosten I, Netea M, van der Ven A: Translating the role of vitamin D3 in infectious diseases. Crit Rev Microbiol 2012, 38:122–135.CrossRefPubMed Khoo AL, Chai L, Koenen H, Joosten I, Netea M, van der Ven A: Translating the role of vitamin D3 in infectious diseases. Crit Rev Microbiol 2012, 38:122–135.CrossRefPubMed
19.
20.
go back to reference Horiuchi H, Nagata I, Komoriya K: Protective effect of vitamin D3 analogues on endotoxin shock in mice. Agents Actions 1991, 33:343–348.CrossRefPubMed Horiuchi H, Nagata I, Komoriya K: Protective effect of vitamin D3 analogues on endotoxin shock in mice. Agents Actions 1991, 33:343–348.CrossRefPubMed
21.
go back to reference Djukic M, Onken ML, Schütze S, Redlich S, Götz A, Hanisch UK, Bertsch T, Ribes S, Hanenberg A, Schneider S, Bollheimer C, Sieber C, Nau R: Vitamin D deficiency reduces the immune response, phagocytosis rate, and intracellular killing rate of microglial cells. Infect Immun 2014, 82:2585–2594.PubMedCentralCrossRefPubMed Djukic M, Onken ML, Schütze S, Redlich S, Götz A, Hanisch UK, Bertsch T, Ribes S, Hanenberg A, Schneider S, Bollheimer C, Sieber C, Nau R: Vitamin D deficiency reduces the immune response, phagocytosis rate, and intracellular killing rate of microglial cells. Infect Immun 2014, 82:2585–2594.PubMedCentralCrossRefPubMed
22.
go back to reference Nau R, Wellmer A, Soto A, Koch K, Schneider O, Schmidt H, Gerber J, Michel U, Brück W: Rifampin reduces early mortality in experimental Streptococcus pneumoniae meningitis. J Infect Dis 1999, 179:1557–1560.CrossRefPubMed Nau R, Wellmer A, Soto A, Koch K, Schneider O, Schmidt H, Gerber J, Michel U, Brück W: Rifampin reduces early mortality in experimental Streptococcus pneumoniae meningitis. J Infect Dis 1999, 179:1557–1560.CrossRefPubMed
23.
go back to reference Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME: Identification and kinetics of leukocytes after severe ischaemia or reperfusion renal injury. Nephrol Dial Transplant 2000, 15:1562–1574.CrossRefPubMed Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME: Identification and kinetics of leukocytes after severe ischaemia or reperfusion renal injury. Nephrol Dial Transplant 2000, 15:1562–1574.CrossRefPubMed
24.
go back to reference Mildner A, Djukic M, Garbe D, Wellmer A, Kuziel WA, Mack M, Nau R, Prinz M: Ly-6G + CCR2 − myeloid cells rather than Ly-6C high CCR2 + monocytes are required for the control of bacterial infection in the central nervous system. J Immunol 2008, 2008(181):2713–2722.CrossRef Mildner A, Djukic M, Garbe D, Wellmer A, Kuziel WA, Mack M, Nau R, Prinz M: Ly-6G + CCR2 myeloid cells rather than Ly-6C high CCR2 + monocytes are required for the control of bacterial infection in the central nervous system. J Immunol 2008, 2008(181):2713–2722.CrossRef
25.
go back to reference Beard JA, Bearden A, Striker R: Vitamin D and the anti-viral state. J Clin Virol 2001, 50:194–200.CrossRef Beard JA, Bearden A, Striker R: Vitamin D and the anti-viral state. J Clin Virol 2001, 50:194–200.CrossRef
26.
go back to reference Lemire JM, Adams JS, Kermani-Arab V, Bakke AC, Sakai R, Jordan SC: 1,25-Dihydroxyvitamin D3 suppresses human T helper/inducer lymphocyte activity in vitro . J Immunol 1985, 134:3032–3035.PubMed Lemire JM, Adams JS, Kermani-Arab V, Bakke AC, Sakai R, Jordan SC: 1,25-Dihydroxyvitamin D3 suppresses human T helper/inducer lymphocyte activity in vitro . J Immunol 1985, 134:3032–3035.PubMed
27.
go back to reference Abbas AK, Murphy KM, Sher A: Functional diversity of helper T lymphocytes. Nature 1996, 383:787–793.CrossRefPubMed Abbas AK, Murphy KM, Sher A: Functional diversity of helper T lymphocytes. Nature 1996, 383:787–793.CrossRefPubMed
29.
go back to reference Prinz M, Kann O, Draheim HJ, Schumann RR, Kettenmann H, Weber JR, Hanisch UK: Microglial activation by components of gram-positive and -negative bacteria: distinct and common routes to the induction of ion channels and cytokines. J Neuropathol Exp Neurol 1999, 58:1078–1089.CrossRefPubMed Prinz M, Kann O, Draheim HJ, Schumann RR, Kettenmann H, Weber JR, Hanisch UK: Microglial activation by components of gram-positive and -negative bacteria: distinct and common routes to the induction of ion channels and cytokines. J Neuropathol Exp Neurol 1999, 58:1078–1089.CrossRefPubMed
30.
go back to reference Ribes S, Regen T, Meister T, Tauber SC, Schütze S, Mildner A, Mack M, Hanisch UK, Nau R: Resistance of the brain to Escherichia coli K1 infection depends on MyD88 signaling and the contribution of neutrophils and monocytes. Infect Immun 2013, 81:1810–1819.PubMedCentralCrossRefPubMed Ribes S, Regen T, Meister T, Tauber SC, Schütze S, Mildner A, Mack M, Hanisch UK, Nau R: Resistance of the brain to Escherichia coli K1 infection depends on MyD88 signaling and the contribution of neutrophils and monocytes. Infect Immun 2013, 81:1810–1819.PubMedCentralCrossRefPubMed
31.
go back to reference Hu W, Nessler S, Hemmer B, Eagar TN, Kane LP, Leliveld SR, Müller-Schiffmann A, Gocke AR, Lovett-Racke A, Ben LH, Hussain RZ, Breil A, Elliott JL, Puttaparthi K, Cravens PD, Singh MP, Petsch B, Stitz L, Racke MK, Korth C, Stüve O: Pharmaco-logical prion protein silencing accelerates central nervous system autoimmune disease via T cell receptor signalling. Brain 2010, 133:375–388.PubMedCentralCrossRefPubMed Hu W, Nessler S, Hemmer B, Eagar TN, Kane LP, Leliveld SR, Müller-Schiffmann A, Gocke AR, Lovett-Racke A, Ben LH, Hussain RZ, Breil A, Elliott JL, Puttaparthi K, Cravens PD, Singh MP, Petsch B, Stitz L, Racke MK, Korth C, Stüve O: Pharmaco-logical prion protein silencing accelerates central nervous system autoimmune disease via T cell receptor signalling. Brain 2010, 133:375–388.PubMedCentralCrossRefPubMed
32.
go back to reference Mitchell AJ, Yau B, McQuillan JA, Ball HJ, Too LK, Abtin A, Hertzog P, Leib SL, Jones CA, Gerega SK, Weninger W, Hunt NH: Inflammasome-dependent IFN-γ drives pathogenesis in Streptococcus pneumonia meningitis. J Immunol 2012, 189:4970–4980.CrossRefPubMed Mitchell AJ, Yau B, McQuillan JA, Ball HJ, Too LK, Abtin A, Hertzog P, Leib SL, Jones CA, Gerega SK, Weninger W, Hunt NH: Inflammasome-dependent IFN-γ drives pathogenesis in Streptococcus pneumonia meningitis. J Immunol 2012, 189:4970–4980.CrossRefPubMed
33.
go back to reference Bergman P, Norlin AC, Hansen S, Rekha RS, Agerberth B, Björkhem-Bergman L, Ekström L, Lindh JD, Andersson J: Vitamin D3 supplementation in patients with frequent respiratory tract infections: a randomised and double-blind intervention study. BMJ Open 2012, 2:e001663.PubMedCentralCrossRefPubMed Bergman P, Norlin AC, Hansen S, Rekha RS, Agerberth B, Björkhem-Bergman L, Ekström L, Lindh JD, Andersson J: Vitamin D3 supplementation in patients with frequent respiratory tract infections: a randomised and double-blind intervention study. BMJ Open 2012, 2:e001663.PubMedCentralCrossRefPubMed
34.
go back to reference Zehnder D, Bland R, Williams MC, McNinch RW, Howie AJ, Stewart PM, Hewison M: Extrarenal expression of 25-hydroxyvitamin D(3)-1a-hydroxylase. J Clin Endocrinol Metab 2001, 86:888–894.PubMed Zehnder D, Bland R, Williams MC, McNinch RW, Howie AJ, Stewart PM, Hewison M: Extrarenal expression of 25-hydroxyvitamin D(3)-1a-hydroxylase. J Clin Endocrinol Metab 2001, 86:888–894.PubMed
35.
go back to reference Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE: Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 2007, 179:1634.CrossRefPubMed Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE: Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 2007, 179:1634.CrossRefPubMed
37.
go back to reference Gombart AF, Borregaard N, Koeffler HP: Human cathelicidin antimicrobial peptide ( CAMP ) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J 2005, 19:1067–1077.CrossRefPubMed Gombart AF, Borregaard N, Koeffler HP: Human cathelicidin antimicrobial peptide ( CAMP ) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J 2005, 19:1067–1077.CrossRefPubMed
38.
go back to reference Ustianowski A, Shaffer R, Collin S, Wilkinson RJ, Davidson RN: Prevalence and associations of vitamin D deficiency in foreign-born persons with tuberculosis in London. J Infect 2005, 50:432–437.CrossRefPubMed Ustianowski A, Shaffer R, Collin S, Wilkinson RJ, Davidson RN: Prevalence and associations of vitamin D deficiency in foreign-born persons with tuberculosis in London. J Infect 2005, 50:432–437.CrossRefPubMed
39.
go back to reference Asakura H, Aoshima K, Suga Y, Yamazaki M, Morishita E, Saito M, Miyamoto K, Nakao S: Beneficial effect of the active form of vitamin D3 against LPS-induced DIC but not against tissue-factor-induced DIC in rat models. Thromb Haemost 2001, 85:287–290.PubMed Asakura H, Aoshima K, Suga Y, Yamazaki M, Morishita E, Saito M, Miyamoto K, Nakao S: Beneficial effect of the active form of vitamin D3 against LPS-induced DIC but not against tissue-factor-induced DIC in rat models. Thromb Haemost 2001, 85:287–290.PubMed
40.
go back to reference Mandell E, Seedorf G, Gien J, Abman SH: Vitamin D treatment improves survival and infant lung structure after intra-amniotic endotoxin exposure in rats: potential role for the prevention of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2014, 306:L420–L428.PubMedCentralCrossRefPubMed Mandell E, Seedorf G, Gien J, Abman SH: Vitamin D treatment improves survival and infant lung structure after intra-amniotic endotoxin exposure in rats: potential role for the prevention of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2014, 306:L420–L428.PubMedCentralCrossRefPubMed
41.
go back to reference Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zügel U, Gallo RL, Eisenberg D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modlin RL: Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006, 311:1770–1773.CrossRefPubMed Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zügel U, Gallo RL, Eisenberg D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modlin RL: Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006, 311:1770–1773.CrossRefPubMed
42.
go back to reference Risso A: Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J Leukoc Biol 2000, 68:785–792.PubMed Risso A: Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J Leukoc Biol 2000, 68:785–792.PubMed
43.
go back to reference Zanetti M: Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004, 75:39–48.CrossRefPubMed Zanetti M: Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004, 75:39–48.CrossRefPubMed
44.
go back to reference Gombart AF, Saito T, Koeffler HP: Exaptation of an ancient Alu short interspersed element provides a highly conserved vitamin D-mediated innate immune response in humans and primates. BMC Genomics 2009, 10:321.PubMedCentralCrossRefPubMed Gombart AF, Saito T, Koeffler HP: Exaptation of an ancient Alu short interspersed element provides a highly conserved vitamin D-mediated innate immune response in humans and primates. BMC Genomics 2009, 10:321.PubMedCentralCrossRefPubMed
45.
go back to reference Matheu V, Bäck O, Mondoc E, Issazadeh-Navikas S: Dual effects of vitamin D-induced alteration of Th1/Th2 cytokine expression: enhancing IgE production and decreasing airway eosinophilia in murine allergic airway disease. J Allergy Clin Immunol 2003, 112:585–592.CrossRefPubMed Matheu V, Bäck O, Mondoc E, Issazadeh-Navikas S: Dual effects of vitamin D-induced alteration of Th1/Th2 cytokine expression: enhancing IgE production and decreasing airway eosinophilia in murine allergic airway disease. J Allergy Clin Immunol 2003, 112:585–592.CrossRefPubMed
46.
go back to reference Smith JA, Das A, Ray SK, Banik NL: Role of proinflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 2012, 87:10–20.CrossRefPubMed Smith JA, Das A, Ray SK, Banik NL: Role of proinflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 2012, 87:10–20.CrossRefPubMed
48.
go back to reference Hanisch UK, Prinz M, Angstwurm K, Häusler KG, Kann O, Kettenmann H, Weber JR: The protein tyrosine kinase inhibitor AG126 prevents the massive microglial cytokine induction by pneumococcal cell walls. Eur J Immunol 2001, 31:2104–2115.CrossRefPubMed Hanisch UK, Prinz M, Angstwurm K, Häusler KG, Kann O, Kettenmann H, Weber JR: The protein tyrosine kinase inhibitor AG126 prevents the massive microglial cytokine induction by pneumococcal cell walls. Eur J Immunol 2001, 31:2104–2115.CrossRefPubMed
49.
go back to reference Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, Lokensgard JR, Peterson PK: Role of microglia in central nervous system infections. Clin Microbiol Rev 2004, 17:942–964.PubMedCentralCrossRefPubMed Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, Lokensgard JR, Peterson PK: Role of microglia in central nervous system infections. Clin Microbiol Rev 2004, 17:942–964.PubMedCentralCrossRefPubMed
50.
go back to reference Braun JS, Novak R, Murray PJ, Eischen CM, Susin SA, Kroemer G, Halle A, Weber JR, Tuomanen EI, Cleveland JL: Apoptosis-inducing factor mediates microglial and neuronal apoptosis caused by pneumococcus. J Infect Dis 2001, 184:1300–1309.CrossRefPubMed Braun JS, Novak R, Murray PJ, Eischen CM, Susin SA, Kroemer G, Halle A, Weber JR, Tuomanen EI, Cleveland JL: Apoptosis-inducing factor mediates microglial and neuronal apoptosis caused by pneumococcus. J Infect Dis 2001, 184:1300–1309.CrossRefPubMed
51.
go back to reference Gerber J, Nau R: Mechanisms of injury in bacterial meningitis. Curr Opin Neurol 2010, 23:312–318.CrossRefPubMed Gerber J, Nau R: Mechanisms of injury in bacterial meningitis. Curr Opin Neurol 2010, 23:312–318.CrossRefPubMed
52.
go back to reference Ramesh G, MacLean AG, Philipp MT: Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediators Inflamm 2013, 2013:480739.PubMedCentralPubMed Ramesh G, MacLean AG, Philipp MT: Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediators Inflamm 2013, 2013:480739.PubMedCentralPubMed
53.
go back to reference Yu X, Zhang X, Zhao B, Wang J, Zhu Z, Teng Z, Shao J, Shen J, Gao Y, Yuan Z, Wu F: Intensive cytokine induction in pandemic H1N1 influenza virus infection accompanied by robust production of IL-10 and IL-6. PLoS ONE 2011, 6:e28680.PubMedCentralCrossRefPubMed Yu X, Zhang X, Zhao B, Wang J, Zhu Z, Teng Z, Shao J, Shen J, Gao Y, Yuan Z, Wu F: Intensive cytokine induction in pandemic H1N1 influenza virus infection accompanied by robust production of IL-10 and IL-6. PLoS ONE 2011, 6:e28680.PubMedCentralCrossRefPubMed
54.
go back to reference Zwijnenburg PJ, Van der Poll T, Florquin S, Roord JJ, Van Furth AM: Interleukin-10 negatively regulates local cytokine and chemokine production but does not influence antibacterial host defense during murine pneumococcal meningitis. Infect Immun 2003, 71:2276–2279.PubMedCentralCrossRefPubMed Zwijnenburg PJ, Van der Poll T, Florquin S, Roord JJ, Van Furth AM: Interleukin-10 negatively regulates local cytokine and chemokine production but does not influence antibacterial host defense during murine pneumococcal meningitis. Infect Immun 2003, 71:2276–2279.PubMedCentralCrossRefPubMed
55.
go back to reference Orihuela CJ, Fillon S, Smith-Sielicki SH, El Kasmi KC, Gao G, Soulis K, Patil A, Murray PJ, Tuomanen EI: Cell wall-mediated neuronal damage in early sepsis. Infect Immun 2006, 74:3783–3789.PubMedCentralCrossRefPubMed Orihuela CJ, Fillon S, Smith-Sielicki SH, El Kasmi KC, Gao G, Soulis K, Patil A, Murray PJ, Tuomanen EI: Cell wall-mediated neuronal damage in early sepsis. Infect Immun 2006, 74:3783–3789.PubMedCentralCrossRefPubMed
56.
go back to reference Koedel U, Bernatowicz A, Frei K, Fontana A, Pfister H-W: Systemically (but not intrathecally) administered IL-10 attenuates pathophysiologic alterations in experimental pneumococcal meningitis. J Immunol 1996, 157:5185–5191.PubMed Koedel U, Bernatowicz A, Frei K, Fontana A, Pfister H-W: Systemically (but not intrathecally) administered IL-10 attenuates pathophysiologic alterations in experimental pneumococcal meningitis. J Immunol 1996, 157:5185–5191.PubMed
Metadata
Title
Vitamin D deficiency decreases survival of bacterial meningoencephalitis in mice
Authors
Marija Djukic
Nadine Sostmann
Thomas Bertsch
Marianne Mecke
Stefan Nessler
Anja Manig
Uwe-Karsten Hanisch
Jakob Triebel
L Cornelius Bollheimer
Cornel Sieber
Roland Nau
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2015
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-014-0208-1

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