Induction of an Inflammatory Loop by Interleukin-1β and Tumor Necrosis Factor-α Involves NF-kB and STAT-1 in Differentiated Human Neuroprogenitor Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Pugazhenthi, Subbiah ^a,b   Zhang, Yuji ^c   Bouchard, Ron ^a,b   Mahaffey, Gregory ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; STAT1 PROTEIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RELEASE; GENETIC ANALYSIS; GLIA CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE TEST; INFLAMMATION; MICROGLIA; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; STEM CELL;

CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; NEURAL STEM CELLS; NF-KAPPA B; STAT1 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880779328     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069585     Document Type: Article

References (48)

1. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH, (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918-934.
2. Tong L, Balazs R, Soiampornkul R, Thangnipon W, Cotman CW, (2008) Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol Aging 29: 1380-1393.
3. Nichol KE, Poon WW, Parachikova AI, Cribbs DH, Glabe CG, et al. (2008) Exercise alters the immune profile in Tg2576 Alzheimer mice toward a response coincident with improved cognitive performance and decreased amyloid. J Neuroinflammation 5: 13.
4. Koo JW, Duman RS, (2008) IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 105: 751-756.
5. Galli R, Gritti A, Bonfanti L, Vescovi AL, (2003) Neural stem cells: an overview. Circ Res 92: 598-608.
6. Bottai D, Fiocco R, Gelain F, Defilippis L, Galli R, et al. (2003) Neural stem cells in the adult nervous system. J Hematother Stem Cell Res 12: 655-670.
7. Velmurugan K, Bouchard R, Mahaffey G, Pugazhenthi S, (2012) Neuroprotective actions of Glucagon-like peptide-1 in differentiated human neuroprogenitor cells. J Neurochem 123: 919-931.
8. Baggiolini M, (2001) Chemokines in pathology and medicine. J Intern Med 250: 91-104.
9. Luster AD, (1998) Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 338: 436-445.
10. de Haas AH, van Weering HR, de Jong EK, Boddeke HW, Biber KP, (2007) Neuronal chemokines: versatile messengers in central nervous system cell interaction. Mol Neurobiol 36: 137-151.
11. Sheng WS, Hu S, Ni HT, Rowen TN, Lokensgard JR, et al. (2005) TNF-alpha-induced chemokine production and apoptosis in human neural precursor cells. J Leukoc Biol 78: 1233-1241.
12. Smale ST, (2012) Transcriptional regulation in the innate immune system. Curr Opin Immunol 24: 51-57.
13. Ryan DA, Narrow WC, Federoff HJ, Bowers WJ, (2010) An improved method for generating consistent soluble amyloid-beta oligomer preparations for in vitro neurotoxicity studies. J Neurosci Methods 190: 171-179.
14. Pugazhenthi S, Wang M, Pham S, Sze CI, Eckman CB, (2011) Downregulation of CREB expression in Alzheimer's brain and in Abeta-treated rat hippocampal neurons. Mol Neurodegener 6: 60.
15. Pugazhenthi S, Phansalkar K, Audesirk G, West A, Cabell L, (2006) Differential regulation of c-jun and CREB by acrolein and 4-hydroxynonenal. Free Radic Biol Med 40: 21-34.
16. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, et al. (2008) Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 93: 4331-4341.
17. Velmurugan K, Balamurugan AN, Loganathan G, Ahmad A, Hering BJ, et al. (2012) Antiapoptotic Actions of Exendin-4 against Hypoxia and Cytokines Are Augmented by CREB. Endocrinology pp. 1116-1128.
18. Majumder S, Zhou LZ, Chaturvedi P, Babcock G, Aras S, et al. (1998) p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha. J Immunol 161: 4736-4744.
19. Jambal P, Masterson S, Nesterova A, Bouchard R, Bergman B, et al. (2003) Cytokine-mediated downregulation of the transcription factor CREB in pancreatic beta-cells. J Biol Chem 278: 23055-23065.
20. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72: 248-254.
21. Zhang Y, Xuan J, de los Reyes BG, Clarke R, Ressom HW, (2008) Network motif-based identification of transcription factor-target gene relationships by integrating multi-source biological data. BMC Bioinformatics 9: 203.
22. Prasad TS, Kandasamy K, Pandey A, (2009) Human Protein Reference Database and Human Proteinpedia as discovery tools for systems biology. Methods Mol Biol 577: 67-79.
23. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-110.
24. Wernicke S, Rasche F, (2006) FANMOD: a tool for fast network motif detection. Bioinformatics 22: 1152-1153.
25. Yeger-Lotem E, Sattath S, Kashtan N, Itzkovitz S, Milo R, et al. (2004) Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. Proc Natl Acad Sci U S A 101: 5934-5939.
26. Pugazhenthi S, Nair S, Velmurugan K, Liang Q, Mahalingam R, et al. (2011) Varicella-zoster virus infection of differentiated human neural stem cells. J Virol 85: 6678-6686.
27. Tenner AJ, (2001) Complement in Alzheimer's disease: opportunities for modulating protective and pathogenic events. Neurobiol Aging 22: 849-861.
28. Sasaki CY, Barberi TJ, Ghosh P, Longo DL, (2005) Phosphorylation of RelA/p65 on serine 536 defines an I{kappa}B{alpha}-independent NF-{kappa}B pathway. J Biol Chem 280: 34538-34547.
29. Duan RS, Yang X, Chen ZG, Lu MO, Morris C, et al. (2008) Decreased fractalkine and increased IP-10 expression in aged brain of APP(swe) transgenic mice. Neurochem Res 33: 1085-1089.
30. Wyss-Coray T, (2006) Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 12: 1005-1015.
31. Shaftel SS, Griffin WS, O'Banion MK, (2008) The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J Neuroinflammation 5: 7.
32. Ray B, Lahiri DK, (2009) Neuroinflammation in Alzheimer's disease: different molecular targets and potential therapeutic agents including curcumin. Curr Opin Pharmacol 9: 434-444.
33. Bhat NR, (2010) Linking cardiometabolic disorders to sporadic Alzheimer's disease: a perspective on potential mechanisms and mediators. J Neurochem 115: 551-562.
34. Alon U, (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
35. Liu T, Clark RK, McDonnell PC, Young PR, White RF, et al. (1994) Tumor necrosis factor-alpha expression in ischemic neurons. Stroke 25: 1481-1488.
36. Murphy PG, Grondin J, Altares M, Richardson PM, (1995) Induction of interleukin-6 in axotomized sensory neurons. J Neurosci 15: 5130-5138.
37. Kumar M, Verma S, Nerurkar VR, (2010) Pro-inflammatory cytokines derived from West Nile virus (WNV)-infected SK-N-SH cells mediate neuroinflammatory markers and neuronal death. J Neuroinflammation 7: 73.
38. Wu X, Lu Y, Dong Y, Zhang G, Zhang Y, et al. (2012) The inhalation anesthetic isoflurane increases levels of proinflammatory TNF-alpha, IL-6, and IL-1beta. Neurobiol Aging 33: 1364-1378.
39. Janelsins MC, Mastrangelo MA, Park KM, Sudol KL, Narrow WC, et al. (2008) Chronic neuron-specific tumor necrosis factor-alpha expression enhances the local inflammatory environment ultimately leading to neuronal death in 3×Tg-AD mice. Am J Pathol 173: 1768-1782.
40. van Weering HR, Boddeke HW, Vinet J, Brouwer N, de Haas AH, et al. (2011) CXCL10/CXCR3 signaling in glia cells differentially affects NMDA-induced cell death in CA and DG neurons of the mouse hippocampus. Hippocampus 21: 220-232.
41. Glaser J, Gonzalez R, Sadr E, Keirstead HS, (2006) Neutralization of the chemokine CXCL10 reduces apoptosis and increases axon sprouting after spinal cord injury. J Neurosci Res 84: 724-734.
42. Pugazhenthi U, Velmurugan K, Tran A, Mahaffey G, Pugazhenthi S, (2010) Anti-inflammatory action of exendin-4 in human islets is enhanced by phosphodiesterase inhibitors: potential therapeutic benefits in diabetic patients. Diabetologia 53: 2357-2368.
43. Christen U, Von Herrath MG, (2004) IP-10 and type 1 diabetes: a question of time and location. Autoimmunity 37: 273-282.
44. Schulthess FT, Paroni F, Sauter NS, Shu L, Ribaux P, et al. (2009) CXCL10 impairs beta cell function and viability in diabetes through TLR4 signaling. Cell Metab 9: 125-139.
45. Vukic V, Callaghan D, Walker D, Lue LF, Liu QY, et al. (2009) Expression of inflammatory genes induced by beta-amyloid peptides in human brain endothelial cells and in Alzheimer's brain is mediated by the JNK-AP1 signaling pathway. Neurobiol Dis 34: 95-106.
46. Shen Q, Zhang R, Bhat NR, (2006) MAP kinase regulation of IP10/CXCL10 chemokine gene expression in microglial cells. Brain Res 1086: 9-16.
47. Moore F, Naamane N, Colli ML, Bouckenooghe T, Ortis F, et al. (2011) STAT1 is a master regulator of pancreatic {beta}-cell apoptosis and islet inflammation. J Biol Chem 286: 929-941.
48. Hindlycke H, Lu T, Welsh N, (2012) Cytokine-induced human islet cell death in vitro correlates with a persistently high phosphorylation of STAT-1, but not with NF-kappaB activation. Biochem Biophys Res Commun 418: 845-850.