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Published in: Journal of Neuroinflammation 1/2018

Open Access 01-12-2018 | Research

Activin A increases phagocytosis of Escherichia coli K1 by primary murine microglial cells activated by toll-like receptor agonists

Authors: Catharina Diesselberg, Sandra Ribes, Jana Seele, Annika Kaufmann, Sandra Redlich, Stephanie Bunkowski, Uwe-Karsten Hanisch, Uwe Michel, Roland Nau, Sandra Schütze

Published in: Journal of Neuroinflammation | Issue 1/2018

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Abstract

Background

Bacterial meningitis is associated with high mortality and long-term neurological sequelae. Increasing the phagocytic activity of microglia could improve the resistance of the CNS against infections. We studied the influence of activin A, a member of the TGF-β family with known immunoregulatory and neuroprotective effects, on the functions of microglial cells in vitro.

Methods

Primary murine microglial cells were treated with activin A (0.13 ng/ml–13 μg/ml) alone or in combination with agonists of TLR2, 4, and 9. Phagocytosis of Escherichia coli K1 as well as release of TNF-α, IL-6, CXCL1, and NO was assessed.

Results

Activin A dose-dependently enhanced the phagocytosis of Escherichia coli K1 by microglial cells activated by agonists of TLR2, 4, and 9 without further increasing NO and proinflammatory cytokine release. Cell viability of microglial cells was not affected by activin A.

Conclusions

Priming of microglial cells with activin A could increase the elimination of bacteria in bacterial CNS infections. This preventive strategy could improve the resistance of the brain to infections, particularly in elderly and immunocompromised patients.
Literature
1.
go back to reference Nau R, Djukic M, Spreer A, Ribes S, Eiffert H. Bacterial meningitis: an update of new treatment options. Expert Rev Anti-Infect Ther. 2015;13:1401–23.CrossRefPubMed Nau R, Djukic M, Spreer A, Ribes S, Eiffert H. Bacterial meningitis: an update of new treatment options. Expert Rev Anti-Infect Ther. 2015;13:1401–23.CrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference Cabellos C, Verdaguer R, Olmo M, Fernández-Sabé N, Cisnal M, Ariza J, et al. Community-acquired bacterial meningitis in elderly patients: experience over 30 years. Medicine (Balitmore). 2009;88:115–9.CrossRef Cabellos C, Verdaguer R, Olmo M, Fernández-Sabé N, Cisnal M, Ariza J, et al. Community-acquired bacterial meningitis in elderly patients: experience over 30 years. Medicine (Balitmore). 2009;88:115–9.CrossRef
5.
go back to reference Kim KS. Strategy of Escherichia coli for crossing the blood-brain barrier. J Infect Dis. 2002;186:220–4.CrossRef Kim KS. Strategy of Escherichia coli for crossing the blood-brain barrier. J Infect Dis. 2002;186:220–4.CrossRef
7.
go back to reference Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2000;2:675–80.CrossRef Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2000;2:675–80.CrossRef
8.
go back to reference Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol. 2002;61:1013–21.CrossRefPubMed Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol. 2002;61:1013–21.CrossRefPubMed
9.
go back to reference Perry VH, Newman TA, Cunningham C. The impact of systemic infection on the progression of neurodegenerative disease. Nat Rev Neurosci. 2003;4:103–12.CrossRefPubMed Perry VH, Newman TA, Cunningham C. The impact of systemic infection on the progression of neurodegenerative disease. Nat Rev Neurosci. 2003;4:103–12.CrossRefPubMed
11.
go back to reference Takeda K, Kaisho T, Akira S. Toll-like receptors. Ann Rev Immunol. 2003;21:335–76.CrossRef Takeda K, Kaisho T, Akira S. Toll-like receptors. Ann Rev Immunol. 2003;21:335–76.CrossRef
12.
go back to reference Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282:2085–8.CrossRefPubMed Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282:2085–8.CrossRefPubMed
13.
go back to reference Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740–5.CrossRefPubMed Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740–5.CrossRefPubMed
14.
go back to reference Smith ME, van der Maesen K, Somera FP. Macrophage and microglial responses to cytokines in vitro: phagocytic activity, proteolytic enzyme release, and free radical production. J Neurosci Res. 1998;54:68–78.CrossRefPubMed Smith ME, van der Maesen K, Somera FP. Macrophage and microglial responses to cytokines in vitro: phagocytic activity, proteolytic enzyme release, and free radical production. J Neurosci Res. 1998;54:68–78.CrossRefPubMed
15.
go back to reference Häusler KG, Prinz M, Nolte C, Weber JR, Schumann RR, Kettenmann H, et al. Interferon-gamma differentially modulates the release of cytokines and chemokines in lipopolysaccharide- and pneumococcal cell wall-stimulated mouse microglia and macrophages. Eur J Neurosci. 2002;16:2113–22.CrossRefPubMed Häusler KG, Prinz M, Nolte C, Weber JR, Schumann RR, Kettenmann H, et al. Interferon-gamma differentially modulates the release of cytokines and chemokines in lipopolysaccharide- and pneumococcal cell wall-stimulated mouse microglia and macrophages. Eur J Neurosci. 2002;16:2113–22.CrossRefPubMed
16.
go back to reference Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387–94.CrossRefPubMed Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387–94.CrossRefPubMed
17.
go back to reference Schütze S, Ribes S, Kaufmann A, Manig A, Scheffel J, Redlich S, et al. Higher mortality and impaired elimination of bacteria in aged mice after intracerebral infection with E. coli are associated with an age-related decline of microglia and macrophage functions. Oncotarget. 2014;5:12573–92.CrossRefPubMedPubMedCentral Schütze S, Ribes S, Kaufmann A, Manig A, Scheffel J, Redlich S, et al. Higher mortality and impaired elimination of bacteria in aged mice after intracerebral infection with E. coli are associated with an age-related decline of microglia and macrophage functions. Oncotarget. 2014;5:12573–92.CrossRefPubMedPubMedCentral
18.
go back to reference Ribes S, Ebert S, Czesnik D, Regen T, Zeug A, Bukowski S, et al. Toll-like receptor prestimulation increases phagocytosis of Escherichia coli DH5alpha and Escherichia coli K1 strains by murine microglial cells. Infect Immun. 2009;77:557–64.CrossRefPubMed Ribes S, Ebert S, Czesnik D, Regen T, Zeug A, Bukowski S, et al. Toll-like receptor prestimulation increases phagocytosis of Escherichia coli DH5alpha and Escherichia coli K1 strains by murine microglial cells. Infect Immun. 2009;77:557–64.CrossRefPubMed
19.
go back to reference Ebert S, Gerber J, Bader S, Mühlhauser F, Brechtel K, Mitchell TJ, et al. Dose-dependent activation of microglial cells by toll-like receptor agonists alone and in combination. J Neuroimmunol. 2005;159:87–96.CrossRefPubMed Ebert S, Gerber J, Bader S, Mühlhauser F, Brechtel K, Mitchell TJ, et al. Dose-dependent activation of microglial cells by toll-like receptor agonists alone and in combination. J Neuroimmunol. 2005;159:87–96.CrossRefPubMed
20.
go back to reference Redlich S, Ribes S, Schütze S, Eiffert H, Nau R. Toll-like receptor stimulation increases phagocytosis of Cryptococcus neoformans by microglial cells. J Neuroinflamm. 2013;10:71.CrossRef Redlich S, Ribes S, Schütze S, Eiffert H, Nau R. Toll-like receptor stimulation increases phagocytosis of Cryptococcus neoformans by microglial cells. J Neuroinflamm. 2013;10:71.CrossRef
21.
go back to reference Chao CC, Hu S, Close K, Choi CS, Molitor TW, Novick WJ, et al. Cytokine release from microglia: differential inhibition by pentoxifylline and dexamethasone. J Infect Dis. 1992;166:847–53.CrossRefPubMed Chao CC, Hu S, Close K, Choi CS, Molitor TW, Novick WJ, et al. Cytokine release from microglia: differential inhibition by pentoxifylline and dexamethasone. J Infect Dis. 1992;166:847–53.CrossRefPubMed
22.
go back to reference Dawson VL, Brahmbhatt HP, Mong JA, Dawson TM. Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal-glial cortical cultures. Neuropharmacology. 1994;33:1425–30.CrossRefPubMed Dawson VL, Brahmbhatt HP, Mong JA, Dawson TM. Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal-glial cortical cultures. Neuropharmacology. 1994;33:1425–30.CrossRefPubMed
23.
go back to reference Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003;100:8514–9.CrossRefPubMedPubMedCentral Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003;100:8514–9.CrossRefPubMedPubMedCentral
24.
go back to reference Iliev AI, Stringaris AK, Nau R, Neumann H. Neuronal injury mediated via stimulation of microglial toll-like receptor-9 (TLR9). FASEB J. 2004;18:412–4.CrossRefPubMed Iliev AI, Stringaris AK, Nau R, Neumann H. Neuronal injury mediated via stimulation of microglial toll-like receptor-9 (TLR9). FASEB J. 2004;18:412–4.CrossRefPubMed
25.
go back to reference Schütze S, Loleit T, Zeretzke M, Bunkowski S, Brück W, Ribes S, et al. Additive microglia-mediated neuronal injury caused by amyloid-β and bacterial TLR agonists in murine neuron-microglia co-cultures quantified by an automated image analysis using cognition network technology. J Alzheimers Dis. 2012;31:651–7.CrossRefPubMed Schütze S, Loleit T, Zeretzke M, Bunkowski S, Brück W, Ribes S, et al. Additive microglia-mediated neuronal injury caused by amyloid-β and bacterial TLR agonists in murine neuron-microglia co-cultures quantified by an automated image analysis using cognition network technology. J Alzheimers Dis. 2012;31:651–7.CrossRefPubMed
26.
go back to reference Redlich S, Ribes S, Schütze S, Nau R. Palmitoylethanolamide stimulates phagocytosis of Escherichia coli K1 by macrophages and increases the resistance of mice against infections. J Neuroinflamm. 2014;11:108.CrossRef Redlich S, Ribes S, Schütze S, Nau R. Palmitoylethanolamide stimulates phagocytosis of Escherichia coli K1 by macrophages and increases the resistance of mice against infections. J Neuroinflamm. 2014;11:108.CrossRef
27.
go back to reference Nau R, Ribes S, Djukic M, Eiffert H. Strategies to increase the activity of microglia as efficient protectors of the brain against infections. Front Cell Neurosci. 2014;8:138.CrossRefPubMedPubMedCentral Nau R, Ribes S, Djukic M, Eiffert H. Strategies to increase the activity of microglia as efficient protectors of the brain against infections. Front Cell Neurosci. 2014;8:138.CrossRefPubMedPubMedCentral
28.
go back to reference Ebert S, Nau R, Michel U. Role of activin in bacterial infection: a potential target for immunointervention? Immunotherapy. 2010;2:673–84.CrossRefPubMed Ebert S, Nau R, Michel U. Role of activin in bacterial infection: a potential target for immunointervention? Immunotherapy. 2010;2:673–84.CrossRefPubMed
29.
go back to reference Chen W, Ten Dijke P. Immunoregulation by members of the TGFβ superfamily. Nat Rev Immunol. 2016;16:723–40.CrossRefPubMed Chen W, Ten Dijke P. Immunoregulation by members of the TGFβ superfamily. Nat Rev Immunol. 2016;16:723–40.CrossRefPubMed
30.
go back to reference Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, et al. Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature. 1986;321:776–9.CrossRefPubMed Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, et al. Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature. 1986;321:776–9.CrossRefPubMed
31.
go back to reference Phillips DJ, de Kretser DM, Hedger MP. Activin and related proteins in inflammation: not just interested bystanders. Cytokine Growth Factor Rev. 2009;20:153–64.CrossRefPubMed Phillips DJ, de Kretser DM, Hedger MP. Activin and related proteins in inflammation: not just interested bystanders. Cytokine Growth Factor Rev. 2009;20:153–64.CrossRefPubMed
32.
go back to reference Michel U, Ebert S, Phillips D, Nau R. Serum concentrations of activin and follistatin are elevated and run parallel in patients with septicemia. Eur J Endocrinol. 2003;148:559–64.CrossRefPubMed Michel U, Ebert S, Phillips D, Nau R. Serum concentrations of activin and follistatin are elevated and run parallel in patients with septicemia. Eur J Endocrinol. 2003;148:559–64.CrossRefPubMed
33.
go back to reference Michel U, Ebert S, Schneider O, Shintani Y, Bunkowski S, Smirnov A, et al. Follistatin (FS) in human cerebrospinal fluid and regulation of FS expression in a mouse model of meningitis. Eur J Endocrinol. 2000;143:809–16.CrossRefPubMed Michel U, Ebert S, Schneider O, Shintani Y, Bunkowski S, Smirnov A, et al. Follistatin (FS) in human cerebrospinal fluid and regulation of FS expression in a mouse model of meningitis. Eur J Endocrinol. 2000;143:809–16.CrossRefPubMed
34.
go back to reference Ebert S, Phillips DJ, Jenzewski P, Nau R, O’Connor AE, Michel U. Activin A concentrations in human cerebrospinal fluid are age-dependent and elevated in meningitis. J Neurol Sci. 2006;250:50–7.CrossRefPubMed Ebert S, Phillips DJ, Jenzewski P, Nau R, O’Connor AE, Michel U. Activin A concentrations in human cerebrospinal fluid are age-dependent and elevated in meningitis. J Neurol Sci. 2006;250:50–7.CrossRefPubMed
35.
go back to reference Ebert S, Zeretzke M, Nau R, Michel U. Microglial cells and peritoneal macrophages release activin A upon stimulation with toll-like receptor agonists. Neurosci Lett. 2007;413:241–4.CrossRefPubMed Ebert S, Zeretzke M, Nau R, Michel U. Microglial cells and peritoneal macrophages release activin A upon stimulation with toll-like receptor agonists. Neurosci Lett. 2007;413:241–4.CrossRefPubMed
36.
go back to reference Wilms H, Schwark T, Brandenburg L, Sievers J, Dengler R, Deuschl G, et al. Regulation of activin A synthesis in microglial cells: pathophysiological implications for bacterial meningitis. J Neurosci Res. 2010;88:16–23.CrossRefPubMed Wilms H, Schwark T, Brandenburg L, Sievers J, Dengler R, Deuschl G, et al. Regulation of activin A synthesis in microglial cells: pathophysiological implications for bacterial meningitis. J Neurosci Res. 2010;88:16–23.CrossRefPubMed
37.
go back to reference Abdipranoto-Cowley A, Park JS, Croucher D, Daniel J, Henshall S, Galbraith S, Mervin K, Vissel B. Activin A is essential for neurogenesis following neurodegeneration. Stem Cells. 2009;27:1330–46.CrossRefPubMedPubMedCentral Abdipranoto-Cowley A, Park JS, Croucher D, Daniel J, Henshall S, Galbraith S, Mervin K, Vissel B. Activin A is essential for neurogenesis following neurodegeneration. Stem Cells. 2009;27:1330–46.CrossRefPubMedPubMedCentral
38.
go back to reference Ge J, Wang Y, Feng Y, Liu H, Cui X, Chen F, et al. Direct effects of activin A on the activation of mouse macrophages RAW264.7 cells. Cell Mol Immunol. 2009;6:129–33.CrossRefPubMedPubMedCentral Ge J, Wang Y, Feng Y, Liu H, Cui X, Chen F, et al. Direct effects of activin A on the activation of mouse macrophages RAW264.7 cells. Cell Mol Immunol. 2009;6:129–33.CrossRefPubMedPubMedCentral
39.
go back to reference Wang Y, Cui X, Tai G, Ge J, Li N, Chen F, et al. A critical role of activin A in maturation of mouse peritoneal macrophages in vitro and in vivo. Cell Mol Immunol. 2009;6:387–9.CrossRefPubMedPubMedCentral Wang Y, Cui X, Tai G, Ge J, Li N, Chen F, et al. A critical role of activin A in maturation of mouse peritoneal macrophages in vitro and in vivo. Cell Mol Immunol. 2009;6:387–9.CrossRefPubMedPubMedCentral
40.
go back to reference Li N, Cui X, Ge J, Li J, Niu L, Liu H, et al. Activin A inhibits activities of lipopolysaccharide-activated macrophages via TLR4, not of TLR 2. Biochem Biophys Res Commun. 2013;435:222–8.CrossRefPubMed Li N, Cui X, Ge J, Li J, Niu L, Liu H, et al. Activin A inhibits activities of lipopolysaccharide-activated macrophages via TLR4, not of TLR 2. Biochem Biophys Res Commun. 2013;435:222–8.CrossRefPubMed
41.
go back to reference Zhou J, Tai G, Liu H, Ge J, Feng Y, Chen F, et al. Activin A down-regulates the phagocytosis of lipopolysaccharide-activated mouse peritoneal macrophages in vitro and in vivo. Cell Immunol. 2009;255:69–75.CrossRefPubMed Zhou J, Tai G, Liu H, Ge J, Feng Y, Chen F, et al. Activin A down-regulates the phagocytosis of lipopolysaccharide-activated mouse peritoneal macrophages in vitro and in vivo. Cell Immunol. 2009;255:69–75.CrossRefPubMed
42.
go back to reference Park SE, Lee J, Chang EH, Kim JH, Sung J-H, Na DL, et al. Activin A secreted by human mesenchymal stem cells induces neuronal development and neurite outgrowth in an in vitro model of Alzheimer’s disease: neurogenesis induced by MSCs via activin A. Arch Pharm Res. 2016;39:1171–9.CrossRefPubMed Park SE, Lee J, Chang EH, Kim JH, Sung J-H, Na DL, et al. Activin A secreted by human mesenchymal stem cells induces neuronal development and neurite outgrowth in an in vitro model of Alzheimer’s disease: neurogenesis induced by MSCs via activin A. Arch Pharm Res. 2016;39:1171–9.CrossRefPubMed
43.
go back to reference Mukerji S, Rainey RN, Rhodes J, Hall A. Delayed activin A administration attenuates tissue death after transient focal cerebral ischemia and is associated with decreased stress-responsive kinase activation. J Neurochem. 2009;111:1138–48.CrossRefPubMedPubMedCentral Mukerji S, Rainey RN, Rhodes J, Hall A. Delayed activin A administration attenuates tissue death after transient focal cerebral ischemia and is associated with decreased stress-responsive kinase activation. J Neurochem. 2009;111:1138–48.CrossRefPubMedPubMedCentral
44.
go back to reference Stayte S, Rentsch P, Tröscher AR, Bamberger M, Li KM, Vissel B. Activin A inhibits MPTP and LPS-induced increases in inflammatory cell populations and loss of dopamine neurons in the mouse midbrain in vivo. PLoS One. 2017;12:e0167211.CrossRefPubMedPubMedCentral Stayte S, Rentsch P, Tröscher AR, Bamberger M, Li KM, Vissel B. Activin A inhibits MPTP and LPS-induced increases in inflammatory cell populations and loss of dopamine neurons in the mouse midbrain in vivo. PLoS One. 2017;12:e0167211.CrossRefPubMedPubMedCentral
45.
go back to reference Phillips DJ, Nguyen P, Adamides AA, Bye N, Rosenfeld JV, Kossmann T, et al. Activin A release into cerebrospinal fluid in a subset of patients with severe traumatic brain injury. J Neurotrauma. 2006;23:1283–94.CrossRefPubMed Phillips DJ, Nguyen P, Adamides AA, Bye N, Rosenfeld JV, Kossmann T, et al. Activin A release into cerebrospinal fluid in a subset of patients with severe traumatic brain injury. J Neurotrauma. 2006;23:1283–94.CrossRefPubMed
46.
go back to reference Pardridge WM. Advances in cell biology of blood-brain barrier transport. Semin Cell Biol. 1991;2:419–26.PubMed Pardridge WM. Advances in cell biology of blood-brain barrier transport. Semin Cell Biol. 1991;2:419–26.PubMed
47.
48.
go back to reference Wang S, Tai G, Zhang P, Mu D, Zhang X, Liu Z. Inhibitory effect of activin A on activation of lipopolysaccharide-stimulated mouse macrophage RAW264.7 cells. Cytokine. 2008;42:85–91.CrossRefPubMed Wang S, Tai G, Zhang P, Mu D, Zhang X, Liu Z. Inhibitory effect of activin A on activation of lipopolysaccharide-stimulated mouse macrophage RAW264.7 cells. Cytokine. 2008;42:85–91.CrossRefPubMed
49.
go back to reference Mitchell K, Shah JP, Tsytsikova LV, Campbell AM, Affram K, Symes AJ. LPS antagonism of TGF-β signaling results in prolonged survival and activation of rat primary microliga. J Neurochem. 2014;129:155–68.CrossRefPubMed Mitchell K, Shah JP, Tsytsikova LV, Campbell AM, Affram K, Symes AJ. LPS antagonism of TGF-β signaling results in prolonged survival and activation of rat primary microliga. J Neurochem. 2014;129:155–68.CrossRefPubMed
50.
go back to reference Nüsing RM, Barsig J. Induction of prostanoid, nitric oxide, and cytokine formation in rat bone marrow derived macrophages by activin A. Br J Pharmacol. 1999;127:919–26.CrossRefPubMedPubMedCentral Nüsing RM, Barsig J. Induction of prostanoid, nitric oxide, and cytokine formation in rat bone marrow derived macrophages by activin A. Br J Pharmacol. 1999;127:919–26.CrossRefPubMedPubMedCentral
51.
go back to reference Zhang XJ, Li Y, Tai GX, Xu GY, Zhang PY, Yang Y, et al. Effects of activin A on the activities of the mouse peritoneal macrophages. Cell Mol Immunol. 2005;2:63–7.PubMed Zhang XJ, Li Y, Tai GX, Xu GY, Zhang PY, Yang Y, et al. Effects of activin A on the activities of the mouse peritoneal macrophages. Cell Mol Immunol. 2005;2:63–7.PubMed
Metadata
Title
Activin A increases phagocytosis of Escherichia coli K1 by primary murine microglial cells activated by toll-like receptor agonists
Authors
Catharina Diesselberg
Sandra Ribes
Jana Seele
Annika Kaufmann
Sandra Redlich
Stephanie Bunkowski
Uwe-Karsten Hanisch
Uwe Michel
Roland Nau
Sandra Schütze
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2018
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-018-1209-2

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