Acetate reduces microglia inflammatory signaling in vitro

Journal of Neurochemistry

Volumn 123, Issue 4, 2012, Pages 555-567

  Soliman, Mahmoud L ^a   Puig, Kendra L ^a   Combs, Colin K ^a   Rosenberger, Thad A ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

acetylation; cytokine; histone; MAPK; microglia; neuroinflammation

Indexed keywords

ACETIC ACID; CYTOKINE; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN; SERINE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ACETYLATION; AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LYSATE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HISTONE ACETYLATION; HYPERACETYLATION; HYPOACETYLATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTRACELLULAR SIGNALING; MICROGLIA; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACETATES; ACETYLATION; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CELLS, CULTURED; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; HISTONES; L-LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDES; LYSINE; MICE; MICE, INBRED C57BL; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84867576303     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07955.x     Document Type: Article

References (74)

1. Adcock I. M., (2007) HDAC inhibitors as anti-inflammatory agents. Br. J. Pharmacol. 150, 829-831.
2. Annunziato A. T., Eason M. B., and, Perry C. A., (1995) Relationship between methylation and acetylation of arginine-rich histones in cycling and arrested HeLa cells. Biochemistry 34, 2916-2924.
3. Ariyannur P. S., Moffett J. R., Madhavarao C. N., Arun P., Vishnu N., Jacobowitz D. M., Hallows W. C., Denu J. M., and, Namboodiri A. M., (2010) Nuclear-cytoplasmic localization of acetyl coenzyme a synthetase-1 in the rat brain. J. Comp. Neurol. 518, 2952-2977.
4. Arun P., Ariyannur P. S., Moffett J. R., Xing G., Hamilton K., Grunberg N. E., Ives J. A., and, Namboodiri A. M., (2010a) Metabolic acetate therapy for the treatment of traumatic brain injury. J. Neurotrauma 27, 293-298.
5. Arun P., Madhavarao C. N., Moffett J. R., et al,. (2010b) Metabolic acetate therapy improves phenotype in the tremor rat model of Canavan disease. J. Inherit. Metab. Dis. 33, 195-210.
6. Atkins C. M., Nozaki N., Shigeri Y., and, Soderling T. R., (2004) Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J. Neurosci. 24, 5193-5201.
7. Beyaert R., Cuenda A., Vanden Berghe W., Plaisance S., Lee J. C., Haegeman G., Cohen P., and, Fiers W., (1996) The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 15, 1914-1923.
8. Blasi E., Barluzzi R., Bocchini V., Mazzolla R., and, Bistoni F., (1990) Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 27, 229-237.
9. Bocchini V., Mazzolla R., Barluzzi R., Blasi E., Sick P., and, Kettenmann H., (1992) An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res. 31, 616-621.
10. Cao W., Bao C., Padalko E., and, Lowenstein C. J., (2008) Acetylation of mitogen-activated protein kinase phosphatase-1 inhibits Toll-like receptor signaling. J. Exp. Med. 205, 1491-1503.
11. Chen F. E., and, Ghosh G., (1999) Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views. Oncogene 18, 6845-6852.
12. Chen L., Fischle W., Verdin E., and, Greene W. C., (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293, 1653-1657.
13. Chen L. F., Mu Y., and, Greene W. C., (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J. 21, 6539-6548.
14. Chen J., Zhou Y., Mueller-Steiner S., Chen L. F., Kwon H., Yi S., Mucke L., and, Gan L., (2005) SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J. Biol. Chem. 280, 40364-40374.
15. Denes A., Thornton P., Rothwell N. J., and, Allan S. M., (2010) Inflammation and brain injury: acute cerebral ischaemia, peripheral and central inflammation. Brain Behav. Immun. 24, 708-723.
16. Dhandapani K. M., and, Brann D. W., (2003) Transforming growth factor-beta: a neuroprotective factor in cerebral ischemia. Cell Biochem. Biophys. 39, 13-22.
17. Dhawan G., Floden A. M., and, Combs C. K., (2012) Amyloid-beta oligomers stimulate microglia through a tyrosine kinase dependent mechanism. Neurobiol. Aging 33, 2247-2261.
18. Fujino T., Kondo J., Ishikawa M., Morikawa K., and, Yamamoto T. T., (2001) Acetyl-CoA synthetase 2, a mitochondrial matrix enzyme involved in the oxidation of acetate. J. Biol. Chem. 276, 11420-11426.
19. Furlan R., Bergami A., Lang R., Brambilla E., Franciotta D., Martinelli V., Comi G., Panina P., and, Martino G., (2000) Interferon-beta treatment in multiple sclerosis patients decreases the number of circulating T cells producing interferon-gamma and interleukin-4. J. Neuroimmunol. 111, 86-92.
20. Galbiati L., Mendoza-Maldonado R., Gutierrez M. I., and, Giacca M., (2005) Regulation of E2F-1 after DNA damage by p300-mediated acetylation and ubiquitination. Cell Cycle 4, 930-939.
21. Glozak M. A., Sengupta N., Zhang X., and, Seto E., (2005) Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23.
22. Govindarajan N., Agis-Balboa R. C., Walter J., Sananbenesi F., and, Fischer A., (2011) Sodium butyrate improves memory function in an Alzheimer's disease mouse model when administered at an advanced stage of disease progression. J. Alzheimers Dis. 26, 187-197.
23. Gregio A. P., Cano V. P., Avaca J. S., Valentini S. R., and, Zanelli C. F., (2009) eIF5A has a function in the elongation step of translation in yeast. Biochem. Biophys. Res. Commun. 380, 785-790.
24. Hanisch U. K., and, Kettenmann H., (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394.
25. Helmy A., De Simoni M. G., Guilfoyle M. R., Carpenter K. L., and, Hutchinson P. J., (2011) Cytokines and innate inflammation in the pathogenesis of human traumatic brain injury. Prog. Neurobiol. 95, 352-372.
26. Hopkins S. J., and, Rothwell N. J., (1995) Cytokines and the nervous system. I: Expression and recognition. Trends Neurosci. 18, 83-88.
27. Hu W., Ralay Ranaivo H., Roy S. M., Behanna H. A., Wing L. K., Munoz L., Guo L., Van Eldik L. J., and, Watterson D. M., (2007) Development of a novel therapeutic suppressor of brain proinflammatory cytokine up-regulation that attenuates synaptic dysfunction and behavioral deficits. Bioorg. Med. Chem. Lett. 17, 414-418.
28. Huang B., Yang X. D., Lamb A., and, Chen L. F., (2010) Posttranslational modifications of NF-kappaB: another layer of regulation for NF-kappaB signaling pathway. Cell. Signal. 22, 1282-1290.
29. Ishfaq M., Maeta K., Maeda S., Natsume T., Ito A., and, Yoshida M., (2012) Acetylation regulates subcellular localization of eukaryotic translation initiation factor 5A (eIF5A). FEBS Lett. doi: 10.1016/j.febslet.2012.06.042.
30. Jeong J. W., Bae M. K., Ahn M. Y., et al,. (2002) Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 111, 709-720.
31. Johnston H., Boutin H., and, Allan S. M., (2011) Assessing the contribution of inflammation in models of Alzheimer's disease. Biochem. Soc. Trans. 39, 886-890.
32. Kiernan R., Bres V., Ng R. W., Coudart M. P., El Messaoudi S., Sardet C., Jin D. Y., Emiliani S., and, Benkirane M., (2003) Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65. J. Biol. Chem. 278, 2758-2766.
33. Kohn D. T., Tsai K. C., Cansino V. V., Neve R. L., and, Perrone-Bizzozero N. I., (1996) Role of highly conserved pyrimidine-rich sequences in the 3' untranslated region of the GAP-43 mRNA in mRNA stability and RNA-protein interactions. Brain Res. Mol. Brain Res. 36, 240-250.
34. Kotlyarov A., Neininger A., Schubert C., Eckert R., Birchmeier C., Volk H. D., and, Gaestel M., (1999) MAPKAP kinase 2 is essential for LPS-induced TNF-alpha biosynthesis. Nat. Cell Biol. 1, 94-97.
35. Kraatz J., Clair L., Bellingham J., Wahlstrom K., Rodriguez J. L., and, West M. A., (1998) Lipopolysaccharide pretreatment produces macrophage endotoxin tolerance via a serum-independent pathway. J. Trauma 45, 684-691.
36. Kumar S., Boehm J., and, Lee J. C., (2003) p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat. Rev. Drug Discov. 2, 717-726.
37. Langley B., Gensert J. M., Beal M. F., and, Ratan R. R., (2005) Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents. Curr. Drug Targets CNS Neurol. Disord. 4, 41-50.
38. Ledeboer A., Breve J. J., Poole S., Tilders F. J., and, Van Dam A. M., (2000) Interleukin-10, interleukin-4, and transforming growth factor-beta differentially regulate lipopolysaccharide-induced production of pro-inflammatory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells. Glia 30, 134-142.
39. Lee S. B., Park J. H., Folk J. E., Deck J. A., Pegg A. E., Sokabe M., Fraser C. S., and, Park M. H., (2011) Inactivation of eukaryotic initiation factor 5A (eIF5A) by specific acetylation of its hypusine residue by spermidine/spermine acetyltransferase 1 (SSAT1). Biochem. J. 433, 205-213.
40. Lehnardt S., (2010) Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58, 253-263.
41. Li Y., Liu L., Barger S. W., and, Griffin W. S., (2003) Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J. Neurosci. 23, 1605-1611.
42. Lloyd E., Somera-Molina K., Van Eldik L. J., Watterson D. M., and, Wainwright M. S., (2008) Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J. Neuroinflammation 5, 28.
43. Mathew R., Arun P., Madhavarao C. N., Moffett J. R., and, Namboodiri M. A., (2005) Progress toward acetate supplementation therapy for Canavan disease: glyceryl triacetate administration increases acetate, but not N-acetylaspartate, levels in brain. J. Pharmacol. Exp. Ther. 315, 297-303.
44. Mendez R., and, Richter J. D., (2001) Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2, 521-529.
45. Merson T. D., Binder M. D., and, Kilpatrick T. J., (2010) Role of cytokines as mediators and regulators of microglial activity in inflammatory demyelination of the CNS. Neuromolecular Med. 12, 99-132.
46. Pearson G., Robinson F., Beers Gibson T., Xu B. E., Karandikar M., Berman K., and, Cobb M. H., (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183.
47. Perkins N. D., Felzien L. K., Betts J. C., Leung K., Beach D. H., and, Nabel G. J., (1997) Regulation of NF-kappaB by cyclin-dependent kinases associated with the p300 coactivator. Science 275, 523-527.
48. Petrova T. V., Akama K. T., and, Van Eldik L. J., (1999) Selective modulation of BV-2 microglial activation by prostaglandin E(2). Differential effects on endotoxin-stimulated cytokine induction. J. Biol. Chem. 274, 28823-28827.
49. Qian L., Flood P. M., and, Hong J. S., (2010) Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J. Neural Transm. 117, 971-979.
50. Ransohoff R. M., and, Perry V. H., (2009) Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145.
51. Reisenauer C. J., Bhatt D. P., Mitteness D. J., Slanczka E. R., Gienger H. M., Watt J. A., and, Rosenberger T. A., (2011) Acetate supplementation attenuates lipopolysaccharide-induced neuroinflammation. J. Neurochem. 117, 264-274.
52. Rice J. C., and, Allis C. D., (2001) Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13, 263-273.
53. Rojanathammanee L., Murphy E. J., and, Combs C. K., (2011) Expression of mutant alpha-synuclein modulates microglial phenotype in vitro. J. Neuroinflammation 8, 44.
54. Rothwell N. J., and, Hopkins S. J., (1995) Cytokines and the nervous system II: Actions and mechanisms of action. Trends Neurosci. 18, 130-136.
55. Sadoul K., Boyault C., Pabion M., and, Khochbin S., (2008) Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie 90, 306-312.
56. Saini P., Eyler D. E., Green R., and, Dever T. E., (2009) Hypusine-containing protein eIF5A promotes translation elongation. Nature 459, 118-121.
57. Sawada M., Suzumura A., Hosoya H., Marunouchi T., and, Nagatsu T., (1999) Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 72, 1466-1471.
58. Schumann R. R., Pfeil D., Lamping N., Kirschning C., Scherzinger G., Schlag P., Karawajew L., and, Herrmann F., (1996) Lipopolysaccharide induces the rapid tyrosine phosphorylation of the mitogen-activated protein kinases erk-1 and p38 in cultured human vascular endothelial cells requiring the presence of soluble CD14. Blood 87, 2805-2814.
59. Seo D. R., Kim K. Y., and, Lee Y. B., (2004) Interleukin-10 expression in lipopolysaccharide-activated microglia is mediated by extracellular ATP in an autocrine fashion. NeuroReport 15, 1157-1161.
60. Shapiro L., and, Dinarello C. A., (1995) Osmotic regulation of cytokine synthesis in vitro. Proc. Natl Acad. Sci. USA 92, 12230-12234.
61. Shin J. H., Li R. W., Gao Y., Baldwin R., and, t. and Li, C. J., (2012) Genome-wide ChIP-seq mapping and analysis reveal butyrate-induced acetylation of H3K9 and H3K27 correlated with transcription activity in bovine cells. Funct. Integr. Genomics 12, 119-130.
62. Silva P. F., Garcia V. A., Dornelles Ada S., et al,. (2012) Memory impairment induced by brain iron overload is accompanied by reduced H3K9 acetylation and ameliorated by sodium butyrate. Neuroscience 200, 42-49.
63. Soliman M. L., and, Rosenberger T. A., (2011) Acetate supplementation increases brain histone acetylation and inhibits histone deacetylase activity and expression. Mol. Cell. Biochem. 352, 173-180.
64. Soliman M. L., Smith M. D., Houdek H. M., and, Rosenberger T. A., (2012) Acetate supplementation modulates brain histone acetylation and decreases interleukin-1beta expression in a rat model of neuroinflammation. J. Neuroinflammation 9, 51.
65. Strahl B. D., and, Allis C. D., (2000) The language of covalent histone modifications. Nature 403, 41-45.
66. Streit W. J., Walter S. A., and, Pennell N. A., (1999) Reactive microgliosis. Prog. Neurobiol. 57, 563-581.
67. Suzuki S., Tanaka K., and, Suzuki N., (2009) Ambivalent aspects of interleukin-6 in cerebral ischemia: inflammatory versus neurotrophic aspects. J. Cereb. Blood Flow Metab. 29, 464-479.
68. Theis M., Si K., and, Kandel E. R., (2003) Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc. Natl Acad. Sci. USA 100, 9602-9607.
69. Vitkovic L., Maeda S., and, Sternberg E., (2001) Anti-inflammatory cytokines: expression and action in the brain. NeuroImmunoModulation 9, 295-312.
70. Vucetic Z., Kimmel J., and, Reyes T. M., (2011) Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology: official publication of the American College of. Neuropsychopharmacology 36, 1199-1206.
71. Wells D. G., (2006) RNA-binding proteins: a lesson in repression. J. Neurosci. 26, 7135-7138.
72. Woo M. S., Jang P. G., Park J. S., Kim W. K., Joh T. H., and, Kim H. S., (2003) Selective modulation of lipopolysaccharide-stimulated cytokine expression and mitogen-activated protein kinase pathways by dibutyryl-cAMP in BV2 microglial cells. Brain Res. Mol. Brain Res. 113, 86-96.
73. Zanelli C. F., Maragno A. L., Gregio A. P., Komili S., Pandolfi J. R., Mestriner C. A., Lustri W. R., and, Valentini S. R., (2006) eIF5A binds to translational machinery components and affects translation in yeast. Biochem. Biophys. Res. Commun. 348, 1358-1366.
74. Zhang B., West E. J., Van K. C., Gurkoff G. G., Zhou J., Zhang X. M., Kozikowski A. P., and, Lyeth B. G., (2008) HDAC inhibitor increases histone H3 acetylation and reduces microglia inflammatory response following traumatic brain injury in rats. Brain Res. 1226, 181-191.