Reciprocal modulation of C/EBP-α and C/EBP-β by IL-13 in activated microglia prevents neuronal death

European Journal of Immunology

Volumn 43, Issue 11, 2013, Pages 2854-2865

  Pan, Hung Chuan ^a,b   Yang, Cheng Ning ^a   Hung, Yi Wen ^b,c   Lee, Wen Jane ^b   Tien, Hsing Ru ^c   Shen, Chin Chang ^d   Sheehan, Jason ^e   Chou, Chiang Ting ^f   Sheu, Meei Ling ^b,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d INSTITUTE OF NUCLEAR ENERGY RESEARCH   (Taiwan)

^e UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^f CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

C EBP; IL 13; Microglia; Neuron

Indexed keywords

CALPAIN; CASPASE 12; CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; CD11B ANTIGEN; CYCLOOXYGENASE 2; HEME OXYGENASE 1; INTERLEUKIN 13; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL DEATH; CONFOCAL MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GEL MOBILITY SHIFT ASSAY; IMMUNOCHEMISTRY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

C/EBP; IL-13; MICROGLIA; NEURON;

ANIMALS; APOPTOSIS; CALPAIN; CASPASE 12; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CCAAT-ENHANCER-BINDING PROTEINS; CELLS, CULTURED; CYCLOOXYGENASE 2; DINOPROSTONE; HEME OXYGENASE-1; INTERLEUKIN-13; LIPOPOLYSACCHARIDES; MEMBRANE PROTEINS; MICROGLIA; NEURONS; PPAR GAMMA; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84888046070     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343301     Document Type: Article

References (50)

1. Smith, J. A., Das, A., Ray, S. K. and Banik, N. L., Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull. 2012. 87: 10-20.
2. Matus, S., Glimcher, L. H. and Hetz, C., Protein folding stress in neurodegenerative diseases: a glimpse into the ER. Curr. Opin. Cell. Biol. 2011. 23: 239-252.
3. Lehotsky, J., Kaplan, P., Babusikova, E., Strapkova, A. and Murin, R., Molecular pathways of endoplasmic reticulum dysfunctions: possible cause of cell death in the nervous system. Physiol. Res. 2003. 52: 269-274.
4. Paschen, W. and Mengesdorf, T., Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium 2005. 38: 409-415.
5. Liu, S. H., Yang, C. N., Pan, H. C., Sung, Y. J., Liao, K. K., Chen, W. B., Lin, W. Z. et al., IL-13 downregulates PPAR-gamma/heme oxygenase-1 via ER stress-stimulated calpain activation: aggravation of activated microglia death. Cell. Mol. Life Sci. 2010. 67: 1465-1476.
6. Yang, M. S., Ji, K. A., Jeon, S. B., Jin, B. K., Kim, S. U., Jou, I. and Joe, E., Interleukin-13 enhances cyclooxygenase-2 expression in activated rat brain microglia: implications for death of activated microglia. J. Immunol. 2006. 177: 1323-1329.
7. Kawahara, K., Suenobu, M., Yoshida, A., Koga, K., Hyodo, A., Ohtsuka, H., Kuniyasu, A. et al., Intracerebral microinjection of interleukin-4/interleukin-13 reduces beta-amyloid accumulation in the ipsilateral side and improves cognitive deficits in young amyloid precursor protein 23 mice. Neuroscience 2012. 207: 243-260.
8. Straccia, M., Gresa-Arribas, N., Dentesano, G., Ejarque-Ortiz, A., Tusell, J. M., Serratosa, J., Sola, C. et al., Pro-inflammatory gene expression and neurotoxic effects of activated microglia are attenuated by absence of CCAAT/enhancer binding protein beta. J. Neuroinflammation 2011. 8: 156.
9. Ejarque-Ortiz, A., Tusell, J. M., Serratosa, J. and Saura, J., CCAAT/enhancer binding protein-alpha is down-regulated by toll-like receptor agonists in microglial cells. J. Neurosci. Res. 2007. 85: 985-993.
10. Yang, M. S., Park, E. J., Sohn, S., Kwon, H. J., Shin, W. H., Pyo, H. K., Jin, B. et al., Interleukin-13 and -4 induce death of activated microglia. Glia 2002. 38: 273-280.
11. Szczepanik, A. M., Funes, S., Petko, W. and Ringheim, G. E., IL-4, IL-10 and IL-13 modulate A beta(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J. Neuroimmunol. 2001. 113: 49-62.
12. Zurawski, G. and de Vries, J. E., Interleukin 13 elicits a subset of the activities of its close relative interleukin 4. Stem Cells 1994. 12: 169-174.
13. Shin, W. H., Lee, D. Y., Park, K. W., Kim, S. U., Yang, M. S., Joe, E. H. and Jin, B. K., Microglia expressing interleukin-13 undergo cell death and contribute to neuronal survival in vivo. Glia 2004. 46: 142-152.
14. Akundi, R. S., Candelario-Jalil, E., Hess, S., Hull, M., Lieb, K., Gebicke-Haerter, P. J. and Fiebich, B. L., Signal transduction pathways regulating cyclooxygenase-2 in lipopolysaccharide-activated primary rat microglia. Glia 2005. 51: 199-208.
15. Won, J. S., Im, Y. B., Khan, M., Singh, A. K. and Singh, I., Involvement of phospholipase A2 and lipoxygenase in lipopolysaccharide-induced inducible nitric oxide synthase expression in glial cells. Glia 2005. 51: 13-21.
16. Sun, G. Y., Xu, J., Jensen, M. D., Yu, S., Wood, W. G., Gonzalez, F. A., Simonyi, A. et al., Phospholipase A2 in astrocytes: responses to oxidative stress, inflammation, and G protein-coupled receptor agonists. Mol. Neurobiol. 2005. 31: 27-41.
17. Goll, D. E., Thompson, V. F., Li, H., Wei, W. and Cong, J., The calpain system. Physiol. Rev. 2003. 83: 731-801.
18. Karmakar, S., Weinberg, M. S., Banik, N. L., Patel, S. J. and Ray, S. K., Activation of multiple molecular mechanisms for apoptosis in human malignant glioblastoma T98G and U87MG cells treated with sulforaphane. Neuroscience 2006. 141: 1265-1280.
19. Sheu, M. L., Liu, S. H. and Lan, K. H., Honokiol induces calpain-mediated glucose-regulated protein-94 cleavage and apoptosis in human gastric cancer cells and reduces tumor growth. PLoS ONE 2007. 2: e1096.
20. Gonen, H., Shkedy, D., Barnoy, S., Kosower, N. S. and Ciechanover, A., On the involvement of calpains in the degradation of the tumor suppressor protein p53. FEBS Lett. 1997. 406: 17-22.
21. Reichrath, J., Welter, C., Mitschele, T., Classen, U., Meineke, V., Tilgen, W. and Seifert, M., Different expression patterns of calpain isozymes 1 and 2 (CAPN1 and 2) in squamous cell carcinomas (SCC) and basal cell carcinomas (BCC) of human skin. J. Pathol. 2003. 199: 509-516.
22. Zalewska, T., Calpain as proposed target for neuroprotective treatment of brain ischemia. Folia Neuropathol. 1996. 34: 121-127.
23. Czogalla, A. and Sikorski, A. F., Spectrin and calpain: a 'target' and a 'sniper' in the pathology of neuronal cells. Cell. Mol. Life Sci. 2005. 62: 1913-1924.
24. Wang, K. K., Calpain and caspase: can you tell the difference? Trends Neurosci. 2000. 23: 20-26.
25. Burguillos, M. A., Hajji, N., Englund, E., Persson, A., Cenci, A. M., Machado, A., Cano, J. et al., Apoptosis-inducing factor mediates dopaminergic cell death in response to LPS-induced inflammatory stimulus: evidence in Parkinson's disease patients. Neurobiol. Dis. 2011. 41: 177-188.
26. Shen, H., Hu, X., Liu, C., Wang, S., Zhang, W., Gao, H., Stetler, R. A. et al., Ethyl pyruvate protects against hypoxic-ischemic brain injury via anti-cell death and anti-inflammatory mechanisms. Neurobiol. Dis. 2010. 37: 711-722.
27. Nakanishi, H., Microglial functions and proteases. Mol. Neurobiol. 2003. 27: 163-176.
28. Levesque, S., Wilson, B., Gregoria, V., Thorpe, L. B., Dallas, S., Polikov, V. S., Hong, J. S. et al., Reactive microgliosis: extracellular micro-calpain and microglia-mediated dopaminergic neurotoxicity. Brain 2010. 133: 808-821.
29. Nerlov, C., C/EBPs: recipients of extracellular signals through proteome modulation. Curr. Opin. Cell. Biol. 2008. 20: 180-185.
30. Nerlov, C., The C/EBP family of transcription factors: a paradigm for interaction between gene expression and proliferation control. Trends Cell. Biol. 2007. 17: 318-324.
31. Valente, T., Mancera, P., Tusell, J. M., Serratosa, J. and Saura, J., C/EBPbeta expression in activated microglia in amyotrophic lateral sclerosis. Neurobiol. Aging 2012. 33: 2186-2199.
32. Dasgupta, S., Jana, M., Liu, X. and Pahan, K., Role of very-late antigen-4 (VLA-4) in myelin basic protein-primed T cell contact-induced expression of proinflammatory cytokines in microglial cells. J. Biol. Chem. 2003. 278: 22424-22431.
33. Kapadia, R., Yi, J. H. and Vemuganti, R., Mechanisms of anti-inflammatory and neuroprotective actions of PPAR-gamma agonists. Front Biosci. 2008. 13: 1813-1826.
34. Schipper, H. M., Heme oxygenase-1: role in brain aging and neurodegeneration. Exp. Gerontol. 2000. 35: 821-830.
35. Otterbein, L. E., Soares, M. P., Yamashita, K. and Bach, F. H., Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 2003. 24: 449-455.
36. Tian, Q., Miyazaki, R., Ichiki, T., Imayama, I., Inanaga, K., Ohtsubo, H., Yano, K. et al., Inhibition of tumor necrosis factor-alpha-induced interleukin-6 expression by telmisartan through cross-talk of peroxisome proliferator-activated receptor-gamma with nuclear factor kappaB and CCAAT/enhancer-binding protein-beta. Hypertension 2009. 53: 798-804.
37. Alam, J., Cai, J. and Smith, A., Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 5' sequences are required for induction by heme or heavy metals. J. Biol. Chem. 1994. 269: 1001-1009.
38. Panguluri, R. C., Long, L. O., Chen, W., Wang, S., Coulibaly, A., Ukoli, F., Jackson, A. et al., COX-2 gene promoter haplotypes and prostate cancer risk. Carcinogenesis 2004. 25: 961-966.
39. Hsieh, P. S., Jin, J. S., Chiang, C. F., Chan, P. C., Chen, C. H. and Shih, K. C., COX-2-mediated inflammation in fat is crucial for obesity-linked insulin resistance and fatty liver. Obesity (Silver. Spring) 2009. 17: 1150-1157.
40. Touqui, L. and aoui-El-Azher, M., Mammalian secreted phospholipases A2 and their pathophysiological significance in inflammatory diseases. Curr. Mol. Med. 2001. 1: 739-754.
41. Geinisman, Y., Disterhoft, J. F., Gundersen, H. J., McEchron, M. D., Persina, I. S., Power, J. M., van der Zee, E. A. et al., Remodeling of hippocampal synapses after hippocampus-dependent associative learning. J. Comp. Neurol. 2000. 417: 49-59.
42. Geinisman, Y., Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 2000. 10: 952-962.
43. McMillan, T. M., Powell, G. E., Janota, I. and Polkey, C. E., Relationships between neuropathology and cognitive functioning in temporal lobectomy patients. J. Neurol. Neurosurg. Psychiatry 1987. 50: 167-176.
44. Cardinal, R. N., Parkinson, J. A., Lachenal, G., Halkerston, K. M., Rudarakanchana, N., Hall, J., Morrison, C. H. et al., Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex and central nucleus of the amygdala on autoshaping performance in rats. Behav. Neurosci. 2002. 116: 553-567.
45. Lee, I., Yoganarasimha, D., Rao, G. and Knierim, J. J., Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 2004. 430: 456-459.
46. Leutgeb, S., Leutgeb, J. K., Barnes, C. A., Moser, E. I., McNaughton, B. L. and Moser, M. B., Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 2005. 309: 619-623.
47. Lee, I. and Kesner, R. P., Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 2004. 14: 301-310.
48. Daumas, S., Halley, H., Frances, B. and Lassalle, J. M., Encoding, consolidation and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn. Mem. 2005. 12: 375-382.
49. Kesner, R. P., Lee, I. and Gilbert, P., A behavioral assessment of hippocampal function based on a subregional analysis. Rev. Neurosci. 2004. 15: 333-351.
50. Martin, S. J., de, H. L. and Morris, R. G., Retrograde amnesia: neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia 2005. 43: 609-624.