Differential effects of lipopolysaccharide on energy metabolism in murine microglial N9 and cholinergic SN56 neuronal cells

Journal of Neurochemistry

Volumn 133, Issue 2, 2015, Pages 284-297

  Klimaszewska ŁAta, Joanna ^a   Gul Hinc, Sylwia ^a   Bielarczyk, Hanna ^a   Ronowska, Anna ^a   Zys̈k, Marlena ^a   Gruzewska, Katarzyna ^a   Pawełczyk, Tadeusz ^a   Szutowicz, Andrzej ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

acetyl CoA; cytotoxicity; lipopolysaccharide; N9 cells; NO; SN56 cells

Indexed keywords

ACETYL COENZYME A; ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; LIPOPOLYSACCHARIDE; NITROGEN OXIDE; OXOGLUTARATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE; TOLL LIKE RECEPTOR; ASPARTIC ACID; CHOLINERGIC RECEPTOR STIMULATING AGENT; CYTOKINE; N-ACETYLASPARTATE; TLR4 PROTEIN, RAT; TOLL LIKE RECEPTOR 4;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL VIABILITY; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ENERGY METABOLISM; ENERGY YIELD; ENZYME INHIBITION; MICROGLIA; MITOCHONDRION; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; NERVE CELL; TRANSFORMED CELL LINE;

MURINAE;

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; ANIMALS; ASPARTIC ACID; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CHOLINERGIC AGENTS; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; NEURONS; TOLL-LIKE RECEPTOR 4;

EID: 84926628914     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12979     Document Type: Article

References (69)

1. Akashi S., Saitoh S. I., Wakabayashi Y., et al,. (2003) Lipopolysaccharide interaction with cell surface Toll-like receptor 4-MD-2: higher affinity than that with MD-2 or CD14. J. Exp. Med. 198, 1035-1042.
2. Banati R. B., Egensperger R., Maassen A., Hager G., Kreutzberg G. W., and, Graeber M. B., (2004) Mitochondria in activated microglia in vitro. J. Neurocytol. 33, 535-541.
3. Baslow M. H., (2007) N-acetylaspartate and N-acetylaspartylglutamate, in Handbook of Neurochemistry and Molecular Biology 3rd Edition, Amino Acids and Peptides in the Nervous System (, Oja S. S., Schousboe A., and, Saransaari P., eds), pp. 305-346 Springer, New York.
4. Beynon A. L., Brown M. R., Wright R., Rees M. I., Sheldon I. M., and, Davies J. S., (2013) Ghrelin inhibits LPS-induced release of IL-6 from mouse dopaminergic neurons. J. Neuroinflammation 10, 40.
5. Bielarczyk H., and, Szutowicz A., (1989) Evidence for the regulatory function of synaptoplasmic acetyl-CoA in acetylcholine synthesis in nerve endings. Biochem. J. 262, 377-380.
6. Bielarczyk H., Jankowska-Kulawy A., Gul S., Pawełczyk T., and, Szutowicz A., (2005) Phenotype dependent differential effects of interleukin-1beta and amyloid-beta on viability and choliner-gic phenotype of T17 neuroblastoma cells. Neurochem. Int. 47, 466-473.
7. Bielarczyk H., Gul S., Ronowska A., Bizon-Zygmańska D., Pawełczyk T., and, Szutowicz A., (2006) RS-alpha-lipoic acid protects cholinergic cells against sodium nitroprusside and amyloid-beta neurotoxicity through restoration of acetyl-CoA level. J. Neurochem. 98, 1242-1251.
8. Bierer L. M., Haroutunian V., Gabriel S., Knott P. J., Carlin L. S., Purohit D. P., Perl D. P., Schmeidler J., Kanof P., and, Davis K. L., (1995) Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits. J. Neurochem. 64, 749-760.
9. Block M. L., Zecca L., and, Hong J. S., (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanism. Nat. Rev. Neurosci. 8, 57-69.
10. Blusztajn J. K., Venturini A., Jackson D. A., Lee H. J., and, Wainer B. H., (1992) Acetylcholine synthesis and release is enhanced by dibutyryl cyclic AMP in a neuronal cell line derived from mouse septum. J. Neurosci. 12, 793-799.
11. Bradford M., (1976) A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
12. Brown G. C., and, Neher J. J., (2010) Inflammatory neurodegeneration and mechanism of microglial killing of neurons. Mol. Neurobiol. 41, 242-247.
13. Brown G. C., and, Neher J. J., (2014) Microglial phagocytosis of live neurons. Nat. Rev. Neurosci. 15, 209-216.
14. Bubber P., Ke Z. J., and, Gibson G. E., (2004) Tricarboxylic acid cycle enzymes following thiamine deficiency. Neurochem. Int. 45, 1021-1028.
15. Bubber P., Haroutunian V., Fisch G., Blass J. P., and, Gibson G. E., (2005) Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann. Neurol. 57, 695-703.
16. Chen Z., Jalabi W., Shpargel K. B., Farabaugh K. T., Dutta R., Yin X., Kidd G. J., Bergmann C. C., Stohlman S. A., and, Trapp B. D., (2012) Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. Neurobiol. Dis. 32, 11706-11715.
17. Chénais B., Morjani H., and, Drapier J. C., (2002) Impact of endogenous nitric oxide on microglial cell energy metabolism and labile iron pool. J. Neurochem. 81, 615-623.
18. Cunningham C., (2013) Microglia and neurodegeneration: the role of systemic inflammation. Glia 61, 71-90.
19. Dodd C. A., and, Filipov N. M., (2011) Manganese potentiates LPS-induced heme-oxygenase 1 in microglia but not dopaminergic cells: role in controlling microglial hydrogen peroxide and inflammatory cytokine output. Neurotoxicology 32, 683-692.
20. Fonnum F., (1975) A rapid radiochemical method for the determination of choline acetyltransferase. J. Neurochem. 24, 407-409.
21. Gibbons H. M., and, Dragunow M., (2006) Microglia induce neural cell death via a proximity-dependent mechanism involving nitric oxide. Brain Res. 1084, 1-15.
22. Gorman M. W., Marble D. R., Ogimoto K., and, Feigl E. O., (2003) Measurement of adenine nucleotides in plasma. Luminescence 18, 173-181.
23. Hammond D. N., Lee H. J., Tonsgard J. H., and, Wainer B. H., (1990) Development and characterization of clonal cell lines derived from septal cholinergic neurons. Brain Res. 512, 190-200.
24. Hassan F., Islam S., Tumurkhuu G., Naiki Y., Koide N., Mori I., Yoshida T., and, Yokoschi T., (2006) Intracellular expression of toll-like receptor 4 in neuroblastoma cells and their unresponsiveness to lipopolysaccharide. BMC Cancer 6, 281.
25. Hines D. J., Choi H. B., Hines R. M., Phillips A. G., and, MacVicar B. A., (2013) Prevention of LPS-induced microglia activation, cytokine production and sickness behavior with TLR4 receptor interfering peptides. PLoS ONE 8, e60388. doi: 10.1371/journal.pone.0060388.
26. Jankowska-Kulawy A., Bielarczyk H., Pawełczyk T., Wrõblewska M., and, Szutowicz A., (2010) Acetyl-CoA deficit in brain mitochondria in experimental thiamine deficiency encephalopathy. Neurochem. Int. 57, 851-856.
27. Jin Y., Sato K., Tobo A., Mogi C., Tobo M., Murata M., Ishii S., In D. S., and, Okajima F., (2014) Inhibition of interleukin-1β production by extracellular acidification though TDAG8/cAMP pathway in mouse microglia. J. Neurochem. 129, 683-695.
28. Jung D. Y., Lee H., Jung B. Y., Ock J., Lee M. S., Lee W. H., and, Suk K., (2005) TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: a critical role of IFN-beta as a decision maker. J. Immunol. 174, 6467-6476.
29. Kalisch B. E., Bock N. A., Davis W. L., and, Rylett R. J., (2002) Inhibitors of nitric oxide synthase attenuate nerve growth factor-mediated increases in choline acetyltransferase expression in PC12 cells. J. Neurochem. 81, 624-635.
30. Klunk W. E., Engler H., Nordberg A., et al,. (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol. 55, 306-319.
31. Koller K. J., Zaczek R., and, Coyle J. T., (1984) N-acetyl-aspartyl-glutamate: regional levels in rat brain and the effects of brain lesions as determined by a new HPLC method. J. Neurochem. 43, 1136-1142.
32. Lehnardt S., Massillon L., Follett P., Jensen F. E., Ratan R., Rosenberg P. A., Volpe J. J., and, Vartanian T., (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl Acad. Sci. USA 100, 8514-8519.
33. Liu B., and, Hong J. S., (2003) Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304, 1-7.
34. Lu X., Ma L., Ruan L., Kong Y., Mou H., Zhang Z., Wang Z., Wang J. M., and, Le Y., (2010) Resveratrol differentially modulates inflammatory responses of microglia and astrocytes. J. Neuroinflammation. 7, 46.
35. Maccioni R. B., Rojo L. E., Fernandez J. A., and, Kuljis R. O., (2009) The role of neuroinflammation in Alzheimer's disease. Ann. N.Y. Acad. Sci. 1153, 240-246.
36. Machova E., Novakova J., Lisa V., and, Doležal V., (2006) Docosahexanoic acid supports cell growth and expression of choline acetyltransferase and muscarinic receptors in NG108-15 cell line. J. Mol. Neurosci. 30, 25-26.
37. McKimmie C. S., Roy D., Forster T., and, Fazakerley J. K., (2006) Innate immune response gene expression profiles of N9 microglia are pathogen-type specific. J. Neuroimmunol. 175, 128-141.
38. Moncada S., and, Bolanos J. P., (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J. Neurochem. 97, 1676-1689.
39. Moss D. W., and, Bates T. E., (2001) Activation of murine microglial cell lines by lipopolysaccharide and interferon-gamma causes NO-mediated decreases in mitochondrial and cellular function. Eur. J. Neurosci. 13, 529-538.
40. Nakamura Y., Si Q. S., and, Kataoka K., (1999) Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci. Res. 35, 95-100.
41. Okun E., Griffioen K. J., and, Mattson M. P., (2011) Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci. 34, 269-281.
42. Olesen O. F., Dago L., and, Mikkelsen J. D., (1998) Amyloid β neurotoxicity in the cholinergic but not in the serotoninergic phenotype of RN46A cells. Mol. Brain Res. 57, 266-274.
43. O'Neill L. A., and, Hardie D. G., (2013) Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 493, 346-355.
44. Pappas B. A., Bayley P. J., Bui B. K., Hansen L. A., and, Thal L. J., (2000) Choline acetyltransferase activity and cognitive domain scores of Alzheimer's patients. Neurobiol. Aging 21, 11-17.
45. Park C. H., Zang H., Sheu K. F. R., Calingasan N. Y., Kristal B. S., Lindsay J. G., and, Gibson G. E., (1999) Metabolic impairment induces oxidative stress, compromises inflammatory responses, and inactivates a key mitochondrial enzyme in microglia. J. Neurochem. 72, 1948-1958.
46. Persson M., and, Ronnback L., (2012) Microglia self-defence mediated through GLT-1 and glutathione. Amino Acids 42, 207-219.
47. Reynolds S. F., and, Blass J. P., (1975) Normal level of acetyl coenzyme A and of acetylcholine in the brains of thiamine-deficient rats. J. Neurochem. 34, 185-186.
48. Ronowska A., Dys̈ A., Jankowska-Kulawy A., Klimaszewska-Łata J., Bielarczyk H., Romianowski P., Pawełczyk T., and, Szutowicz A., (2010) Short-term effects of zinc on acetylcholine metabolism and viability of SN56 cholinergic neuroblastoma cells. Neurochem. Int. 56, 143-151.
49. Schubert P., Ogata T., Marchini C., and, Ferroni S., (2001) Glia-related pathomechanisms in Alzheimer's disease: a therapeutic target? Mech. Ageing Dev. 123, 47-57.
50. Sensi S. L., Paoletti P., Bush A. I., and, Sekler I., (2009) Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 10, 780-792.
51. Sheu K. F. R., Kim Y. T., and, Blass J. P., (1985) An immunological study of the pyruvate dehydrogenase deficit in Alzheimer's disease brain. Ann. Neurol. 17, 444-449.
52. Spector D. L., Goldman R. D., and, Leinwand L. A., (eds) (1998) Cell Laboratory Manual I: Culture and Biochemical Analysis of Cells. pp. 2.8-2.13 Cold Spring Harbor, NY.
53. Szutowicz A., and, Bielarczyk H., (1987) Elimination of CoASH interference from acetyl-CoA assay by maleic anhydride. Anal. Biochem. 164, 292-296.
54. Szutowicz A., Stępień M., and, Piec G., (1981) Determination of pyruvate dehydrogenase and acetyl-CoA synthetase activities using citrate synthase. Anal. Biochem. 115, 81-87.
55. Szutowicz A., Tomaszewicz M., and, Bielarczyk H., (1996) Disturbances of acetyl-CoA, energy and acetylcholine metabolism in some encephalopathies. Acta Neurobiol. Exp. 56, 323-339.
56. Szutowicz A., Tomaszewicz M., Bielarczyk H., and, Jankowska A., (1998) Putative significance of shifts in acetyl-CoA compartmentalization in nerve terminals for disturbances of cholinergic transmission in brain. Dev. Neurosci. 20, 485-492.
57. Szutowicz A., Jankowska A., Blusztajn J. K., and, Tomaszewicz M., (1999) Acetylcholine and acetyl-CoA metabolism in differentiating SN56 septal cell line. J. Neurosci. Res. 57, 131-136.
58. Szutowicz A., Madziar B., Pawełczyk T., Tomaszewicz M., and, Bielarczyk H., (2004) Effects of NGF on acetylcholine, acetyl-CoA metabolism, and viability of differentiated and non-differentiated cholinergic neuroblastoma cells. J. Neurochem. 90, 952-961.
59. Szutowicz A., Bielarczyk H., Gul S., Ronowska A., Pawełczyk T., and, Jankowska-Kulawy A., (2006) Phenotype-dependent susceptibility of cholinergic neuroblastoma cells to neurotoxic inputs. Metab. Brain Dis. 21, 149-161.
60. Szutowicz A., Bielarczyk H., Jankowska-Kulawy A., Pawełczyk T., and, Ronowska A., (2013) Acetyl-CoA the key factor for survival or death of cholinergic neurons in course of neurodegenerative diseases. Neurochem. Res. 38, 1523-1542.
61. Tomaszewicz M., Rossner S., Schliebs R., ?wikowska J., and, Szutowicz A., (2003) Changes incortical acetyl-CoA metabolism after selective basal forebrain cholinergic degeneration by 192IgG-saporin. J. Neurochem. 87, 318-324.
62. Tuček S., (1993) Short-term control of the synthesis of acetylcholine. Prog. Biophys. Mol. Biol. 60, 59-69.
63. Vaisid T., and, Kosower N. S., (2013) Calpastatin is upregulated in non-immune neuronal cells via toll-like receptor 2 (TLR2) pathways by lipid-containing agonists. Biochim. Biophys. Acta 1833, 2369-2377.
64. Visintin A., Mazzoni A., Spitzer J. A., and, Segal D. M., (2001) Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proc. Natl Acad. Sci. USA 98, 12156-12161.
65. Welser-Alves J., and, Milner R., (2013) Microglia are the major source of TNF-α and TGF-β1 in postnatal glial cultures: regulation by cytokines, lipopolysaccharide and vitronectin. Neurochem. Int. 63, 47-53.
66. Xie Z., Wei M., Morgan T. E., Fabrizio P., Han D., Finch C. E., and, Longo V. D., (2002) Peroxynitrite mediates neurotoxicity of amyloid beta-peptide1-42- and lipopolysaccharide-activated microglia. J. Neurosci. 22, 3484-3492.
67. Ye J., Liu Z., Wei J., Lu L., Huang Y., Luo L., and, Xie H., (2013) Protective effect of SIRT1 on toxicity of microglial-derived factors by LPS to PC12 cells via the p53-caspase-3-dependent apoptotic pathway. Neurosci. Lett. 553, 72-77.
68. Zaidi N., Swinnen J. V., and, Smans K., (2012) ATP-citrate lyase: a key player in cancer metabolism. Cancer Res. 72, 3709-3714.
69. Zhao M., Zhou A., Xu L., and, Zhang X., (2014) The role of TLR4-mediated PTEN/PI3K/AKT/NF-κB signaling pathway in neuro-inflammation in hippocampal neurons. Neuroscience 269, 93-101.