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Published in: Journal of Neuroinflammation 1/2015

Open Access 01-12-2015 | Research

Beneficial effect of chronic Staphylococcus aureus infection in a model of multiple sclerosis is mediated through the secretion of extracellular adherence protein

Authors: Prateek Kumar, Benedikt Kretzschmar, Sabine Herold, Roland Nau, Mario Kreutzfeldt, Sandra Schütze, Mathias Bähr, Katharina Hein

Published in: Journal of Neuroinflammation | Issue 1/2015

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Abstract

Background

Bacterial infections have been assumed to worsen multiple sclerosis (MS) disease symptoms and to lead to increased neurodegeneration. However, the underlying biological mechanisms for these effects are complex and poorly understood. Here, we assessed the disease-modulating effects of chronic infection with Staphylococcus aureus, a common human pathogen, on the clinical course and the extent of neurodegeneration in experimental autoimmune encephalomyelitis (EAE), an animal model of MS.

Methods

To conduct this study, we established a persistent chronic infection in female brown Norway rats by inoculating Staphylococcus aureus (S. aureus) bacteria in a subcutaneously implanted tissue cages.

Results

In this study, we observed that the introduction of a localized S. aureus infection during the subclinical phase of EAE induced a chronic systemic inflammatory response, consisting of increased T- and B-cell counts and systemic production of proinflammatory cytokines. Unexpectedly, the S. aureus infection completely prevented the development of clinical EAE, and markedly reduced inflammatory infiltration and demyelination of the optic nerve, while it increased the number of surviving retinal neurons. Using a S. aureus strain that lacked the extracellular adherence protein (Eap), we determined that the extracellular adherence protein is at least partially responsible for the inhibitory effect of S. aureus infection on autoimmune inflammation of the central nervous system.

Conclusions

Our results demonstrate for the first time that chronic infection with S. aureus has a beneficial effect on EAE, indicating a dual role of infection in the pathogenesis of MS. We also showed that secretion of Eap by S. aureus plays a major role in preventing autoimmune inflammation of the CNS. Moreover, we identified Eap as a factor responsible for this protective effect.
Literature
1.
go back to reference Gourraud PA, Harbo HF, Hauser SL, Baranzini SE. The genetics of multiple sclerosis: an up-to-date review. Immunol Rev. 2012;248:87–103.CrossRefPubMed Gourraud PA, Harbo HF, Hauser SL, Baranzini SE. The genetics of multiple sclerosis: an up-to-date review. Immunol Rev. 2012;248:87–103.CrossRefPubMed
2.
go back to reference Craig DW, Goor RM, Wang Z, Paschall J, Ostell J, Feolo M, et al. Assessing and managing risk when sharing aggregate genetic variant data. Nat Rev Genet. 2011;12:730–6.CrossRefPubMedCentralPubMed Craig DW, Goor RM, Wang Z, Paschall J, Ostell J, Feolo M, et al. Assessing and managing risk when sharing aggregate genetic variant data. Nat Rev Genet. 2011;12:730–6.CrossRefPubMedCentralPubMed
3.
go back to reference Willer CJ, Dyment DA, Risch NJ, Sadovnick AD, Ebers GC. Twin concordance and sibling recurrence rates in multiple sclerosis. Proc Natl Acad Sci U S A. 2003;100:12877–82.CrossRefPubMedCentralPubMed Willer CJ, Dyment DA, Risch NJ, Sadovnick AD, Ebers GC. Twin concordance and sibling recurrence rates in multiple sclerosis. Proc Natl Acad Sci U S A. 2003;100:12877–82.CrossRefPubMedCentralPubMed
4.
go back to reference Andersen O, Lygner PE, Bergstrom T, Andersson M, Vahlne A. Viral infections trigger multiple sclerosis relapses: a prospective seroepidemiological study. J Neurol. 1993;240:417–22.CrossRefPubMed Andersen O, Lygner PE, Bergstrom T, Andersson M, Vahlne A. Viral infections trigger multiple sclerosis relapses: a prospective seroepidemiological study. J Neurol. 1993;240:417–22.CrossRefPubMed
5.
go back to reference Du C, Yao SY, Ljunggren-Rose A, Sriram S. Chlamydia pneumoniae infection of the central nervous system worsens experimental allergic encephalitis. J Exp Med. 2002;196:1639–44.CrossRefPubMedCentralPubMed Du C, Yao SY, Ljunggren-Rose A, Sriram S. Chlamydia pneumoniae infection of the central nervous system worsens experimental allergic encephalitis. J Exp Med. 2002;196:1639–44.CrossRefPubMedCentralPubMed
6.
go back to reference Munger KL, Peeling RW, Hernan MA, Chasan-Taber L, Olek MJ, Hankinson SE, et al. Infection with Chlamydia pneumoniae and risk of multiple sclerosis. Epidemiology. 2003;14:141–7.PubMed Munger KL, Peeling RW, Hernan MA, Chasan-Taber L, Olek MJ, Hankinson SE, et al. Infection with Chlamydia pneumoniae and risk of multiple sclerosis. Epidemiology. 2003;14:141–7.PubMed
7.
go back to reference Herrmann I, Kellert M, Schmidt H, Mildner A, Hanisch UK, Bruck W, et al. Streptococcus pneumoniae Infection aggravates experimental autoimmune encephalomyelitis via Toll-like receptor 2. Infect Immun. 2006;74:4841–8.CrossRefPubMedCentralPubMed Herrmann I, Kellert M, Schmidt H, Mildner A, Hanisch UK, Bruck W, et al. Streptococcus pneumoniae Infection aggravates experimental autoimmune encephalomyelitis via Toll-like receptor 2. Infect Immun. 2006;74:4841–8.CrossRefPubMedCentralPubMed
8.
go back to reference Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4615–22.CrossRefPubMedCentralPubMed Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4615–22.CrossRefPubMedCentralPubMed
9.
go back to reference Lehmann D, Ben-Nun A. Bacterial agents protect against autoimmune disease. I. Mice pre-exposed to Bordetella pertussis or Mycobacterium tuberculosis are highly refractory to induction of experimental autoimmune encephalomyelitis. J Autoimmun. 1992;5:675–90.CrossRefPubMed Lehmann D, Ben-Nun A. Bacterial agents protect against autoimmune disease. I. Mice pre-exposed to Bordetella pertussis or Mycobacterium tuberculosis are highly refractory to induction of experimental autoimmune encephalomyelitis. J Autoimmun. 1992;5:675–90.CrossRefPubMed
10.
go back to reference Franca TG, Chiuso-Minicucci F, Zorzella-Pezavento SF, Ishikawa LL, da Rosa LC, Colavite PM, et al. Previous infection with Staphylococcus aureus strains attenuated experimental encephalomyelitis. BMC Neurosci. 2014;15:8.CrossRefPubMedCentralPubMed Franca TG, Chiuso-Minicucci F, Zorzella-Pezavento SF, Ishikawa LL, da Rosa LC, Colavite PM, et al. Previous infection with Staphylococcus aureus strains attenuated experimental encephalomyelitis. BMC Neurosci. 2014;15:8.CrossRefPubMedCentralPubMed
11.
go back to reference Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol. 2007;61:288–99.CrossRefPubMed Ascherio A, Munger KL. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol. 2007;61:288–99.CrossRefPubMed
12.
go back to reference Rau CR, Hein K, Sattler MB, Kretzschmar B, Hillgruber C, McRae BL, et al. Anti-inflammatory effects of FTY720 do not prevent neuronal cell loss in a rat model of optic neuritis. Am J Pathol. 2011;178:1770–81.CrossRefPubMedCentralPubMed Rau CR, Hein K, Sattler MB, Kretzschmar B, Hillgruber C, McRae BL, et al. Anti-inflammatory effects of FTY720 do not prevent neuronal cell loss in a rat model of optic neuritis. Am J Pathol. 2011;178:1770–81.CrossRefPubMedCentralPubMed
13.
go back to reference Meyer R, Weissert R, Diem R, Storch MK, de Graaf KL, Kramer B, et al. Acute neuronal apoptosis in a rat model of multiple sclerosis. J Neurosci. 2001;21:6214–20.PubMed Meyer R, Weissert R, Diem R, Storch MK, de Graaf KL, Kramer B, et al. Acute neuronal apoptosis in a rat model of multiple sclerosis. J Neurosci. 2001;21:6214–20.PubMed
14.
go back to reference Hobom M, Storch MK, Weissert R, Maier K, Radhakrishnan A, Kramer B, et al. Mechanisms and time course of neuronal degeneration in experimental autoimmune encephalomyelitis. Brain Pathol. 2004;14:148–57.CrossRefPubMed Hobom M, Storch MK, Weissert R, Maier K, Radhakrishnan A, Kramer B, et al. Mechanisms and time course of neuronal degeneration in experimental autoimmune encephalomyelitis. Brain Pathol. 2004;14:148–57.CrossRefPubMed
15.
go back to reference Maier K, Kuhnert AV, Taheri N, Sattler MB, Storch MK, Williams SK, et al. Effects of glatiramer acetate and interferon-beta on neurodegeneration in a model of multiple sclerosis: a comparative study. Am J Pathol. 2006;169:1353–64.CrossRefPubMedCentralPubMed Maier K, Kuhnert AV, Taheri N, Sattler MB, Storch MK, Williams SK, et al. Effects of glatiramer acetate and interferon-beta on neurodegeneration in a model of multiple sclerosis: a comparative study. Am J Pathol. 2006;169:1353–64.CrossRefPubMedCentralPubMed
16.
go back to reference Grady M, Cullen JJ. Preventing postoperative Staphylococcus infections: an update. Surg Technol Int. 2003;11:57–60.PubMed Grady M, Cullen JJ. Preventing postoperative Staphylococcus infections: an update. Surg Technol Int. 2003;11:57–60.PubMed
17.
go back to reference Lucet JC, Herrmann M, Rohner P, Auckenthaler R, Waldvogel FA, Lew DP. Treatment of experimental foreign body infection caused by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1990;34:2312–7.CrossRefPubMedCentralPubMed Lucet JC, Herrmann M, Rohner P, Auckenthaler R, Waldvogel FA, Lew DP. Treatment of experimental foreign body infection caused by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1990;34:2312–7.CrossRefPubMedCentralPubMed
18.
go back to reference Duthie ES, Lorenz LL. Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol. 1952;6:95–107.CrossRefPubMed Duthie ES, Lorenz LL. Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol. 1952;6:95–107.CrossRefPubMed
19.
go back to reference Hussain M, von Eiff C, Sinha B, Joost I, Herrmann M, Peters G, et al. Eap Gene as novel target for specific identification of Staphylococcus aureus. J Clin Microbiol. 2008;46:470–6.CrossRefPubMedCentralPubMed Hussain M, von Eiff C, Sinha B, Joost I, Herrmann M, Peters G, et al. Eap Gene as novel target for specific identification of Staphylococcus aureus. J Clin Microbiol. 2008;46:470–6.CrossRefPubMedCentralPubMed
20.
go back to reference Maier K, Merkler D, Gerber J, Taheri N, Kuhnert AV, Williams SK, et al. Multiple neuroprotective mechanisms of minocycline in autoimmune CNS inflammation. Neurobiol Dis. 2007;25:514–25.CrossRefPubMed Maier K, Merkler D, Gerber J, Taheri N, Kuhnert AV, Williams SK, et al. Multiple neuroprotective mechanisms of minocycline in autoimmune CNS inflammation. Neurobiol Dis. 2007;25:514–25.CrossRefPubMed
21.
go back to reference Storch MK, Stefferl A, Brehm U, Weissert R, Wallstrom E, Kerschensteiner M, et al. Autoimmunity to myelin oligodendrocyte glycoprotein in rats mimics the spectrum of multiple sclerosis pathology. Brain Pathol. 1998;8:681–94.CrossRefPubMed Storch MK, Stefferl A, Brehm U, Weissert R, Wallstrom E, Kerschensteiner M, et al. Autoimmunity to myelin oligodendrocyte glycoprotein in rats mimics the spectrum of multiple sclerosis pathology. Brain Pathol. 1998;8:681–94.CrossRefPubMed
22.
go back to reference Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, Flock JI, et al. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med. 2002;8:687–93.CrossRefPubMed Chavakis T, Hussain M, Kanse SM, Peters G, Bretzel RG, Flock JI, et al. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med. 2002;8:687–93.CrossRefPubMed
23.
go back to reference Lee LY, Miyamoto YJ, McIntyre BW, Hook M, McCrea KW, McDevitt D, et al. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J Clin Invest. 2002;110:1461–71.CrossRefPubMedCentralPubMed Lee LY, Miyamoto YJ, McIntyre BW, Hook M, McCrea KW, McDevitt D, et al. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J Clin Invest. 2002;110:1461–71.CrossRefPubMedCentralPubMed
24.
go back to reference Wang H, von Rohrscheidt J, Roehrbein J, Peters T, Sindrilaru A, Kess D, et al. Extracellular adherence protein of Staphylococcus aureus suppresses disease by inhibiting T-cell recruitment in a mouse model of psoriasis. J Invest Dermatol. 2010;130:743–54.CrossRefPubMed Wang H, von Rohrscheidt J, Roehrbein J, Peters T, Sindrilaru A, Kess D, et al. Extracellular adherence protein of Staphylococcus aureus suppresses disease by inhibiting T-cell recruitment in a mouse model of psoriasis. J Invest Dermatol. 2010;130:743–54.CrossRefPubMed
25.
go back to reference Rapp NS, Gilroy J, Lerner AM. Role of bacterial infection in exacerbation of multiple sclerosis. Am J Phys Med Rehabil. 1995;74:415–8.CrossRefPubMed Rapp NS, Gilroy J, Lerner AM. Role of bacterial infection in exacerbation of multiple sclerosis. Am J Phys Med Rehabil. 1995;74:415–8.CrossRefPubMed
26.
go back to reference Edwards S, Zvartau M, Clarke H, Irving W, Blumhardt LD. Clinical relapses and disease activity on magnetic resonance imaging associated with viral upper respiratory tract infections in multiple sclerosis. J Neurol Neurosurg Psychiatry. 1998;64:736–41.CrossRefPubMedCentralPubMed Edwards S, Zvartau M, Clarke H, Irving W, Blumhardt LD. Clinical relapses and disease activity on magnetic resonance imaging associated with viral upper respiratory tract infections in multiple sclerosis. J Neurol Neurosurg Psychiatry. 1998;64:736–41.CrossRefPubMedCentralPubMed
27.
go back to reference Buljevac D, Flach HZ, Hop WC, Hijdra D, Laman JD, Savelkoul HF, et al. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain. 2002;125:952–60.CrossRefPubMed Buljevac D, Flach HZ, Hop WC, Hijdra D, Laman JD, Savelkoul HF, et al. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain. 2002;125:952–60.CrossRefPubMed
28.
go back to reference Buljevac D, Hop WC, Reedeker W, Janssens AC, van der Meche FG, van Doorn PA, et al. Self reported stressful life events and exacerbations in multiple sclerosis: prospective study. BMJ. 2003;327:646.CrossRefPubMedCentralPubMed Buljevac D, Hop WC, Reedeker W, Janssens AC, van der Meche FG, van Doorn PA, et al. Self reported stressful life events and exacerbations in multiple sclerosis: prospective study. BMJ. 2003;327:646.CrossRefPubMedCentralPubMed
29.
go back to reference Kalkers NF, Vrenken H, Uitdehaag BM, Polman CH, Barkhof F. Brain atrophy in multiple sclerosis: impact of lesions and of damage of whole brain tissue. Mult Scler. 2002;8:410–4.CrossRefPubMed Kalkers NF, Vrenken H, Uitdehaag BM, Polman CH, Barkhof F. Brain atrophy in multiple sclerosis: impact of lesions and of damage of whole brain tissue. Mult Scler. 2002;8:410–4.CrossRefPubMed
30.
go back to reference Schiffenbauer J, Johnson HM, Butfiloski EJ, Wegrzyn L, Soos JM. Staphylococcal enterotoxins can reactivate experimental allergic encephalomyelitis. Proc Natl Acad Sci U S A. 1993;90:8543–6.CrossRefPubMedCentralPubMed Schiffenbauer J, Johnson HM, Butfiloski EJ, Wegrzyn L, Soos JM. Staphylococcal enterotoxins can reactivate experimental allergic encephalomyelitis. Proc Natl Acad Sci U S A. 1993;90:8543–6.CrossRefPubMedCentralPubMed
31.
go back to reference Soos JM, Hobeika AC, Butfiloski EJ, Schiffenbauer J, Johnson HM. Accelerated induction of experimental allergic encephalomyelitis in PL/J mice by a non-V beta 8-specific superantigen. Proc Natl Acad Sci U S A. 1995;92:6082–6.CrossRefPubMedCentralPubMed Soos JM, Hobeika AC, Butfiloski EJ, Schiffenbauer J, Johnson HM. Accelerated induction of experimental allergic encephalomyelitis in PL/J mice by a non-V beta 8-specific superantigen. Proc Natl Acad Sci U S A. 1995;92:6082–6.CrossRefPubMedCentralPubMed
32.
go back to reference Moreno B, Jukes JP, Vergara-Irigaray N, Errea O, Villoslada P, Perry VH, et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol. 2011;70:932–42.CrossRefPubMed Moreno B, Jukes JP, Vergara-Irigaray N, Errea O, Villoslada P, Perry VH, et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol. 2011;70:932–42.CrossRefPubMed
33.
go back to reference Sibley WA, Bamford CR, Clark K. Clinical viral infections and multiple sclerosis. Lancet. 1985;1:1313–5.CrossRefPubMed Sibley WA, Bamford CR, Clark K. Clinical viral infections and multiple sclerosis. Lancet. 1985;1:1313–5.CrossRefPubMed
34.
go back to reference Nogai A, Siffrin V, Bonhagen K, Pfueller CF, Hohnstein T, Volkmer-Engert R, et al. Lipopolysaccharide injection induces relapses of experimental autoimmune encephalomyelitis in nontransgenic mice via bystander activation of autoreactive CD4+ cells. J Immunol. 2005;175:959–66.CrossRefPubMed Nogai A, Siffrin V, Bonhagen K, Pfueller CF, Hohnstein T, Volkmer-Engert R, et al. Lipopolysaccharide injection induces relapses of experimental autoimmune encephalomyelitis in nontransgenic mice via bystander activation of autoreactive CD4+ cells. J Immunol. 2005;175:959–66.CrossRefPubMed
35.
go back to reference Visser L. Jan de Heer H, Boven LA, van Riel D, van Meurs M, Melief MJ, et al. Proinflammatory bacterial peptidoglycan as a cofactor for the development of central nervous system autoimmune disease J Immunol. 2005;174:808–16. Visser L. Jan de Heer H, Boven LA, van Riel D, van Meurs M, Melief MJ, et al. Proinflammatory bacterial peptidoglycan as a cofactor for the development of central nervous system autoimmune disease J Immunol. 2005;174:808–16.
36.
go back to reference Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature. 1992;356:63–6.CrossRefPubMed Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, Karin N. Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature. 1992;356:63–6.CrossRefPubMed
37.
go back to reference Archelos JJ, Jung S, Maurer M, Schmied M, Lassmann H, Tamatani T, et al. Inhibition of experimental autoimmune encephalomyelitis by an antibody to the intercellular adhesion molecule ICAM-1. Ann Neurol. 1993;34:145–54.CrossRefPubMed Archelos JJ, Jung S, Maurer M, Schmied M, Lassmann H, Tamatani T, et al. Inhibition of experimental autoimmune encephalomyelitis by an antibody to the intercellular adhesion molecule ICAM-1. Ann Neurol. 1993;34:145–54.CrossRefPubMed
38.
go back to reference Gordon EJ, Myers KJ, Dougherty JP, Rosen H, Ron Y. Both anti-CD11a (LFA-1) and anti-CD11b (MAC-1) therapy delay the onset and diminish the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol. 1995;62:153–60.CrossRefPubMed Gordon EJ, Myers KJ, Dougherty JP, Rosen H, Ron Y. Both anti-CD11a (LFA-1) and anti-CD11b (MAC-1) therapy delay the onset and diminish the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol. 1995;62:153–60.CrossRefPubMed
39.
go back to reference Laschinger M, Vajkoczy P, Engelhardt B. Encephalitogenic T cells use LFA-1 for transendothelial migration but not during capture and initial adhesion strengthening in healthy spinal cord microvessels in vivo. Eur J Immunol. 2002;32:3598–606.CrossRefPubMed Laschinger M, Vajkoczy P, Engelhardt B. Encephalitogenic T cells use LFA-1 for transendothelial migration but not during capture and initial adhesion strengthening in healthy spinal cord microvessels in vivo. Eur J Immunol. 2002;32:3598–606.CrossRefPubMed
40.
go back to reference Xie C, Alcaide P, Geisbrecht BV, Schneider D, Herrmann M, Preissner KT, et al. Suppression of experimental autoimmune encephalomyelitis by extracellular adherence protein of Staphylococcus aureus. J Exp Med. 2006;203:985–94.CrossRefPubMedCentralPubMed Xie C, Alcaide P, Geisbrecht BV, Schneider D, Herrmann M, Preissner KT, et al. Suppression of experimental autoimmune encephalomyelitis by extracellular adherence protein of Staphylococcus aureus. J Exp Med. 2006;203:985–94.CrossRefPubMedCentralPubMed
41.
go back to reference Chavakis T, Preissner KT, Herrmann M. The anti-inflammatory activities of Staphylococcus aureus. Trends Immunol. 2007;28:408–18.CrossRefPubMed Chavakis T, Preissner KT, Herrmann M. The anti-inflammatory activities of Staphylococcus aureus. Trends Immunol. 2007;28:408–18.CrossRefPubMed
42.
go back to reference Harraghy N, Hussain M, Haggar A, Chavakis T, Sinha B, Herrmann M, et al. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology. 2003;149:2701–7.CrossRefPubMed Harraghy N, Hussain M, Haggar A, Chavakis T, Sinha B, Herrmann M, et al. The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology. 2003;149:2701–7.CrossRefPubMed
43.
go back to reference Kalman B, Lublin FD, Lattime E, Joseph J, Knobler RL. Effects of staphylococcal enterotoxin B on T cell receptor V beta utilization and clinical manifestations of experimental allergic encephalomyelitis. J Neuroimmunol. 1993;45:83–8.CrossRefPubMed Kalman B, Lublin FD, Lattime E, Joseph J, Knobler RL. Effects of staphylococcal enterotoxin B on T cell receptor V beta utilization and clinical manifestations of experimental allergic encephalomyelitis. J Neuroimmunol. 1993;45:83–8.CrossRefPubMed
44.
go back to reference Soos JM, Schiffenbauer J, Johnson HM. Treatment of PL/J mice with the superantigen, staphylococcal enterotoxin B, prevents development of experimental allergic encephalomyelitis. J Neuroimmunol. 1993;43:39–43.CrossRefPubMed Soos JM, Schiffenbauer J, Johnson HM. Treatment of PL/J mice with the superantigen, staphylococcal enterotoxin B, prevents development of experimental allergic encephalomyelitis. J Neuroimmunol. 1993;43:39–43.CrossRefPubMed
45.
go back to reference Matsumoto Y, Fujiwara M. Immunomodulation of experimental autoimmune encephalomyelitis by staphylococcal enterotoxin D. Cell Immunol. 1993;149:268–78.CrossRefPubMed Matsumoto Y, Fujiwara M. Immunomodulation of experimental autoimmune encephalomyelitis by staphylococcal enterotoxin D. Cell Immunol. 1993;149:268–78.CrossRefPubMed
46.
go back to reference Kaneider NC, Leger AJ, Kuliopulos A. Therapeutic targeting of molecules involved in leukocyte-endothelial cell interactions. FEBS J. 2006;273:4416–24.CrossRefPubMed Kaneider NC, Leger AJ, Kuliopulos A. Therapeutic targeting of molecules involved in leukocyte-endothelial cell interactions. FEBS J. 2006;273:4416–24.CrossRefPubMed
47.
go back to reference Diem R, Hobom M, Maier K, Weissert R, Storch MK, Meyer R, et al. Methylprednisolone increases neuronal apoptosis during autoimmune CNS inflammation by inhibition of an endogenous neuroprotective pathway. J Neurosci. 2003;23:6993–7000.PubMed Diem R, Hobom M, Maier K, Weissert R, Storch MK, Meyer R, et al. Methylprednisolone increases neuronal apoptosis during autoimmune CNS inflammation by inhibition of an endogenous neuroprotective pathway. J Neurosci. 2003;23:6993–7000.PubMed
Metadata
Title
Beneficial effect of chronic Staphylococcus aureus infection in a model of multiple sclerosis is mediated through the secretion of extracellular adherence protein
Authors
Prateek Kumar
Benedikt Kretzschmar
Sabine Herold
Roland Nau
Mario Kreutzfeldt
Sandra Schütze
Mathias Bähr
Katharina Hein
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/s12974-015-0241-8

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