MAPK and NF-κB Pathways Are Involved in Bisphenol A-Induced TNF-α and IL-6 Production in BV2 Microglial Cells

Inflammation

Volumn 38, Issue 2, 2015, Pages 637-648

  Zhu, Jingying ^a   Jiang, Lei ^c   Liu, Yanqing ^a   Qian, Wenyi ^a   Liu, Jingli ^b   Zhou, Jing ^a   Gao, Rong ^a   Xiao, Hang ^a   Wang, Jun ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

bisphenol A; ER ; immunomodulatory cytokines; MAPK; NF B

Indexed keywords

2-(2-AMINO-3-METHOXYPHENYL)-4H-1-BENZOPYRAN-4-ONE; 4,4' ISOPROPYLIDENEDIPHENOL; ANTHRA(1,9-CD)PYRAZOL-6(2H)-ONE; ANTHRACENE DERIVATIVE; ANTIINFLAMMATORY AGENT; BENZHYDRYL DERIVATIVE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ANTAGONIST; FLAVONOID; FULVESTRANT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PHENOL DERIVATIVE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CYTOLOGY; DEGENERATIVE DISEASE; DRUG EFFECTS; ENZYME ACTIVATION; INFLAMMATION; METABOLISM; MICROGLIA; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTHRACENES; ANTI-INFLAMMATORY AGENTS; BENZHYDRYL COMPOUNDS; CELL LINE; ENDOCRINE DISRUPTORS; ENZYME ACTIVATION; ESTRADIOL; ESTROGEN RECEPTOR ANTAGONISTS; ESTROGEN RECEPTOR MODULATORS; ESTROGENS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; INFLAMMATION; INTERLEUKIN-6; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICROGLIA; NEURODEGENERATIVE DISEASES; NF-KAPPA B; PHENOLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84939881560     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-014-9971-5     Document Type: Article

References (55)

1. Schug, T.T., A. Janesick, B. Blumberg, and J.J. Heindel. 2011. Endocrine disrupting chemicals and disease susceptibility. The Journal of Steroid Biochemistry and Molecular Biology 127: 204–215.
2. Casals-Casas, C., and B. Desvergne. 2011. Endocrine disruptors: from endocrine to metabolic disruption. Annual Review of Physiology 73: 135–162.
3. DiVall, S.A. 2013. The influence of endocrine disruptors on growth and development of children. Current Opinion in Endocrinology Diabetes and Obesity 20: 50–55.
4. Crisp, T.M., E.D. Clegg, R.L. Cooper, W.P. Wood, D.G. Anderson, K.P. Baetcke, J.L. Hoffmann, M.S. Morrow, D.J. Rodier, J.E. Schaeffer, L.W. Touart, M.G. Zeeman, and Y.M. Patel. 1998. Environmental endocrine disruption: an effects assessment and analysis. Environmental Health Perspectives 106(Suppl 1): 11–56.
5. Fernandez, M.F., B. Olmos, A. Granada, M.J. Lopez-Espinosa, J.M. Molina-Molina, J.M. Fernandez, M. Cruz, F. Olea-Serrano, and N. Olea. 2007. Human exposure to endocrine-disrupting chemicals and prenatal risk factors for cryptorchidism and hypospadias: a nested case-control study. Environmental Health Perspectives 115(Suppl 1): 8–14.
6. Elsworth, J.D., J.D. Jentsch, C.A. Vandevoort, R.H. Roth, D.E. Jr, and C. Leranth. 2013. Prenatal exposure to bisphenol A impacts midbrain dopamine neurons and hippocampal spine synapses in non-human primates. Neurotoxicology 35: 113–120.
7. Maffini, M.V., B.S. Rubin, C. Sonnenschein, and A.M. Soto. 2006. Endocrine disruptors and reproductive health: the case of bisphenol-A. Molecular and Cellular Endocrinology 254–255: 179–186.
8. Richter, C.A., L.S. Birnbaum, F. Farabollini, R.R. Newbold, B.S. Rubin, C.E. Talsness, J.G. Vandenbergh, D.R. Walser-Kuntz, and F.S. vom Saal. 2007. In vivo effects of bisphenol A in laboratory rodent studies. Reproductive Toxicology 24: 199–224.
9. Kim, M.E., H.R. Park, E.J. Gong, S.Y. Choi, H.S. Kim, and J. Lee. 2011. Exposure to bisphenol A appears to impair hippocampal neurogenesis and spatial learning and memory. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association 49: 3383–3389.
10. Yang, L., L. Luo, W. Ji, C. Gong, D. Wu, H. Huang, Q. Liu, B. Xia, G. Hu, W. Zhang, Q. Zhang, J. Liu, and Z. Zhuang. 2013. Effect of low dose bisphenol A on the early differentiation of human embryonic stem cells into mammary epithelial cells. Toxicology Letters 218: 187–193.
11. Rogers, J.A., L. Metz, and V.W. Yong. 2013. Review: Endocrine disrupting chemicals and immune responses: a focus on bisphenol-A and its potential mechanisms. Molecular Immunology 53: 421–430.
12. Meeker, J.D., and K.K. Ferguson. 2011. Relationship between urinary phthalate and bisphenol A concentrations and serum thyroid measures in U.S. adults and adolescents from the National Health and Nutrition Examination Survey (NHANES) 2007-2008. Environmental Health Perspectives 119: 1396–1402.
13. Kubo, K., O. Arai, M. Omura, R. Watanabe, R. Ogata, and S. Aou. 2003. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neuroscience Research 45: 345–356.
14. Liu, C., W. Duan, R. Li, S. Xu, L. Zhang, C. Chen, M. He, Y. Lu, H. Wu, H. Pi, X. Luo, Y. Zhang, M. Zhong, Z. Yu, and Z. Zhou. 2013. Exposure to bisphenol A disrupts meiotic progression during spermatogenesis in adult rats through estrogen-like activity. Cell Death and Disease 4: e676.
15. Spence, R.D., A.J. Wisdom, Y. Cao, H.M. Hill, C.R. Mongerson, B. Stapornkul, N. Itoh, M.V. Sofroniew, and R.R. Voskuhl. 2013. Estrogen mediates neuroprotection and anti-inflammatory effects during EAE through ERalpha signaling on astrocytes but not through ERbeta signaling on astrocytes or neurons. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 33: 10924–10933.
16. Gosselin, D., and S. Rivest. 2011. Estrogen receptor transrepresses brain inflammation. Cell 145: 495–497.
17. Spence, R.D., and R.R. Voskuhl. 2012. Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Frontiers in Neuroendocrinology 33: 105–115.
18. Loram, L.C., P.W. Sholar, F.R. Taylor, J.L. Wiesler, J.A. Babb, K.A. Strand, D. Berkelhammer, H.E. Day, S.F. Maier, and L.R. Watkins. 2012. Sex and estradiol influence glial pro-inflammatory responses to lipopolysaccharide in rats. Psychoneuroendocrinology 37: 1688–1699.
19. Graeber, M.B., W. Li, and M.L. Rodriguez. 2011. Role of microglia in CNS inflammation. FEBS Letters 585: 3798–3805.
20. Zhang, W., K. Phillips, A.R. Wielgus, J. Liu, A. Albertini, F.A. Zucca, R. Faust, S.Y. Qian, D.S. Miller, C.F. Chignell, B. Wilson, V. Jackson-Lewis, S. Przedborski, D. Joset, J. Loike, J.S. Hong, D. Sulzer, and L. Zecca. 2011. Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson's disease. Neurotoxicity Research 19: 63–72.
21. Glass, C.K., K. Saijo, B. Winner, M.C. Marchetto, and F.H. Gage. 2010. Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918–934.
22. Glezer, I., A.R. Simard, and S. Rivest. 2007. Neuroprotective role of the innate immune system by microglia. Neuroscience 147: 867–883.
23. Choi, Y., M.K. Lee, S.Y. Lim, S.H. Sung, and Y.C. Kim. 2009. Inhibition of inducible NO synthase, cyclooxygenase-2 and interleukin-1beta by torilin is mediated by mitogen-activated protein kinases in microglial BV2 cells. British Journal of Pharmacology 156: 933–940.
24. Cordle, A., and G. Landreth. 2005. 3-Hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors attenuate beta-amyloid-induced microglial inflammatory responses. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 25: 299–307.
25. Tabb, M.M., and B. Blumberg. 2006. New modes of action for endocrine-disrupting chemicals. Molecular Endocrinology 20: 475–482.
26. Carnevale, D., R. De Simone, and L. Minghetti. 2007. Microglia-neuron interaction in inflammatory and degenerative diseases: role of cholinergic and noradrenergic systems. CNS & Neurological Disorders Drug Targets 6: 388–397.
27. Bhat, N.R., P. Zhang, J.C. Lee, and E.L. Hogan. 1998. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 18: 1633–1641.
28. Roy, A., Y.K. Fung, X. Liu, and K. Pahan. 2006. Up-regulation of microglial CD11b expression by nitric oxide. The Journal of Biological Chemistry 281: 14971–14980.
29. Baker, A.E., V.M. Brautigam, and J.J. Watters. 2004. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor beta. Endocrinology 145: 5021–5032.
30. Laurenzi, M., C. Arcuri, R. Rossi, P. Marconi, and V. Bocchini. 2001. Effects of microenvironment on morphology and function of the microglial cell line BV-2. Neurochemical Research 26: 1209–1216.
31. Glenn, J.A., S.A. Ward, C.R. Stone, P.L. Booth, and W.E. Thomas. 1992. Characterisation of ramified microglial cells: detailed morphology, morphological plasticity and proliferative capability. Journal of Anatomy 180(Pt 1): 109–118.
32. Yamashita, U., T. Sugiura, Y. Yoshida, and E. Kuroda. 2005. Effect of endocrine disrupters on macrophage functions in vitro. Journal of UOEH 27: 1–10.
33. Young Kim, J., and H. Gwang Jeong. 2003. Down-regulation of inducible nitric oxide synthase and tumor necrosis factor-α expression by bisphenol A via nuclear factor-κB inactivation in macrophages. Cancer Letters 196: 69–76.
34. Vandenberg, L.N. 2014. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol a as a case study. Dose-Response 1: 1–18.
35. Wang, H., Q. Wang, U.J. Pape, B. Shen, J. Huang, B. Wu, and X. Li. 2010. Systematic investigation of global coordination among mRNA and protein in cellular society. BMC Genomics 11: 364.
36. Straub, R.H. 2007. The complex role of estrogens in inflammation. Endocrine Reviews 28: 521–574.
37. Vegeto, E., C. Bonincontro, G. Pollio, A. Sala, S. Viappiani, F. Nardi, A. Brusadelli, B. Viviani, P. Ciana, and A. Maggi. 2001. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 21: 1809–1818.
38. Bruce-Keller, A.J., J.L. Keeling, J.N. Keller, F.F. Huang, S. Camondola, and M.P. Mattson. 2000. Antiinflammatory effects of estrogen on microglial activation. Endocrinology 141: 3646–3656.
39. Li, Y., K.A. Burns, Y. Arao, C.J. Luh, and K.S. Korach. 2012. Differential estrogenic actions of endocrine-disrupting chemicals bisphenol A, bisphenol AF, and zearalenone through estrogen receptor alpha and beta in vitro. Environmental Health Perspectives 120: 1029–1035.
40. Hung, C.H., S.N. Yang, P.L. Kuo, Y.T. Chu, H.W. Chang, W.J. Wei, S.K. Huang, and Y.J. Jong. 2010. Modulation of cytokine expression in human myeloid dendritic cells by environmental endocrine-disrupting chemicals involves epigenetic regulation. Environmental Health Perspectives 118: 67–72.
41. Stein, B., and M.X. Yang. 1995. Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Molecular and Cellular Biology 15: 4971–4979.
42. Hirano, S., D. Furutama, and T. Hanafusa. 2007. Physiologically high concentrations of 17beta-estradiol enhance NF-kappaB activity in human T cells. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 292: R1465–R1471.
43. Bulayeva, N.N., B. Gametchu, and C.S. Watson. 2004. Quantitative measurement of estrogen-induced ERK 1 and 2 activation via multiple membrane-initiated signaling pathways. Steroids 69: 181–192.
44. Watson, C.S., N.N. Bulayeva, A.L. Wozniak, and R.A. Alyea. 2007. Xenoestrogens are potent activators of nongenomic estrogenic responses. Steroids 72: 124–134.
45. Cobb, M.H., and E.J. Goldsmith. 1995. How MAP kinases are regulated. Journal of Biological Chemistry 270: 14843–14846.
46. Hohmann, H.P., M. Brockhaus, P.A. Baeuerle, R. Remy, R. Kolbeck, and A.P. van Loon. 1990. Expression of the types A and B tumor necrosis factor (TNF) receptors is independently regulated, and both receptors mediate activation of the transcription factor NF-kappa B. TNF alpha is not needed for induction of a biological effect via TNF receptors. The Journal of Biological Chemistry 265: 22409–22417.
47. Classen, A., B.N. Kalali, C. Schnopp, C. Andres, J.A. Aguilar-Pimentel, J. Ring, M. Ollert, and M. Mempel. 2011. TNF receptor I on human keratinocytes is a binding partner for staphylococcal protein A resulting in the activation of NF kappa B, AP-1, and downstream gene transcription. Experimental Dermatology 20: 48–52.
48. Jongeneel, C.V. 1995. Transcriptional regulation of the tumor necrosis factor α gene. Immunobiology 193: 210–216.
49. Beg, A.A., S.M. Ruben, R.I. Scheinman, S. Haskill, C.A. Rosen, and A.S. Baldwin. 1992. I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention. Genes & Development 6: 1899–1913.
50. Oeckinghaus, A., M.S. Hayden, and S. Ghosh. 2011. Crosstalk in NF-kappaB signaling pathways. Nature Immunology 12: 695–708.
51. Lee, S., Y.K. Kim, T.Y. Shin, and S.H. Kim. 2013. Neurotoxic effects of bisphenol AF on calcium-induced ROS and MAPKs. Neurotoxicity Research 23: 249–259.
52. Cargnello, M., and P.P. Roux. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiology and Molecular Biology Reviews MMBR 75: 50–83.
53. Belcher, S.M., H.H. Le, L. Spurling, and J.K. Wong. 2005. Rapid estrogenic regulation of extracellular signal- regulated kinase 1/2 signaling in cerebellar granule cells involves a G protein- and protein kinase A-dependent mechanism and intracellular activation of protein phosphatase 2A. Endocrinology 146: 5397–5406.
54. Guma, M., D. Stepniak, H. Shaked, M.E. Spehlmann, S. Shenouda, H. Cheroutre, I. Vicente-Suarez, L. Eckmann, M.F. Kagnoff, and M. Karin. 2011. Constitutive intestinal NF-kappaB does not trigger destructive inflammation unless accompanied by MAPK activation. The Journal of Experimental Medicine 208: 1889–1900.
55. Olajide, O.A., M.A. Aderogba, and B.L. Fiebich. 2013. Mechanisms of anti-inflammatory property of Anacardium occidentale stem bark: inhibition of NF-kappaB and MAPK signalling in the microglia. Journal of Ethnopharmacology 145: 42–49.