Microglial HO-1 induction by curcumin provides antioxidant, antineuroinflammatory, and glioprotective effects

Molecular Nutrition and Food Research

Volumn 59, Issue 9, 2015, Pages 1690-1700

  Parada, Esther ^a,b,c   Buendia, Izaskun ^a,b   Navarro, Elisa ^a,b   Avendaño, Carlos ^b   Egea, Javier ^a,b,c   López, Manuela G ^a,b,c  

^a INSTITUTO TEÓFILO HERNANDO   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

Author keywords

Curcumin; Hemoxygenase 1; Inflammation; Microglia; Oxidative stress

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTIOXIDANT; CURCUMIN; HEME OXYGENASE 1; HMOX1 PROTEIN, MOUSE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 4; MEMBRANE PROTEIN; METALLOPORPHYRIN; NOS2 PROTEIN, MOUSE; NOS2 PROTEIN, RAT; PROTOPORPHYRIN; PROTOPORPHYRIN TIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ASTROCYTE; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; MICROGLIA; MOUSE; OXIDATIVE STRESS; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; ASTROCYTES; CURCUMIN; HEME OXYGENASE-1; INTERLEUKIN-4; MEMBRANE PROTEINS; METALLOPORPHYRINS; MICE; MICE, INBRED C57BL; MICROGLIA; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PROTOPORPHYRINS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84942827395     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500279     Document Type: Article

References (59)

1. Maheshwari, R. K., Singh, A. K., Gaddipati, J., Srimal, R. C., Multiple biological activities of curcumin: a short review. Life Sci. 2006, 78, 2081-2087.
2. Gupta, S. C., Patchva, S., Aggarwal, B. B., Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 2013, 15, 195-218.
3. Monroy, A., Lithgow, G. J., Alavez, S., Curcumin and neurodegenerative diseases. Biofactors 2013, 39, 122-132.
4. Hatcher, H., Planalp, R., Cho, J., Torti, F. M. et al., Curcumin: from ancient medicine to current clinical trials. Cell Mol. Life Sci. 2008, 65, 1631-1652.
5. Jagetia, G. C., Aggarwal, B. B., Spicing up of the immune system by curcumin. J. Clin. Immunol. 2007, 27, 19-35.
6. Tsai, Y. M., Chien, C. F., Lin, L. C., Tsai, T. H., Curcumin and its nano-formulation: the kinetics of tissue distribution and blood-brain barrier penetration. Int. J. Pharm. 2011, 416, 331-338.
7. Garcia-Alloza, M., Borrelli, L. A., Rozkalne, A., Hyman, B. T. et al., Curcumin labels amyloid pathology in vivo, disrupts existing plaques, and partially restores distorted neurites in an Alzheimer mouse model. J. Neurochem. 2007, 102, 1095-1104.
8. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J. et al., Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 2005, 280, 5892-5901.
9. Rahman, I., Biswas, S. K., Kirkham, P. A., Regulation of inflammation and redox signaling by dietary polyphenols. Biochem. Pharmacol. 2006, 72, 1439-1452.
10. Aggarwal, B. B., Shishodia, S., Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71, 1397-1421.
11. Hu, P., Huang, P., Chen, M. W., Curcumin attenuates cyclooxygenase-2 expression via inhibition of the NF-kappaB pathway in lipopolysaccharide-stimulated human gingival fibroblasts. Cell Biol. Int. 2013, 37, 443-448.
12. Shishodia, S., Molecular mechanisms of curcumin action: gene expression. Biofactors 2013, 39, 37-55.
13. Hanisch, U. K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10, 1387-1394.
14. Streit, W. J., Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40, 133-139.
15. Qin, L., Liu, Y., Cooper, C., Liu, B. et al., Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J. Neurochem. 2002, 83, 973-983.
16. Allan, S. M., Rothwell, N. J., Cytokines and acute neurodegeneration. Nat. Rev. Neurosci. 2001, 2, 734-744.
17. Schwartz, M., Butovsky, O., Bruck, W., Hanisch, U. K., Microglial phenotype: is the commitment reversible? Trends Neurosci. 2006, 29, 68-74.
18. Block, M. L., Zecca, L., Hong, J. S., Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8, 57-69.
19. Jung, K. K., Lee, H. S., Cho, J. Y., Shin, W. C. et al., Inhibitory effect of curcumin on nitric oxide production from lipopolysaccharide-activated primary microglia. Life Sci. 2006, 79, 2022-2031.
20. Lee, H. S., Jung, K. K., Cho, J. Y., Rhee, M. H. et al., Neuroprotective effect of curcumin is mainly mediated by blockade of microglial cell activation. Pharmazie 2007, 62, 937-942.
21. Zhang, L., Wu, C., Zhao, S., Yuan, D. et al., Demethoxycurcumin, a natural derivative of curcumin attenuates LPS-induced pro-inflammatory responses through down-regulation of intracellular ROS-related MAPK/NF-kappaB signaling pathways in N9 microglia induced by lipopolysaccharide. Int. Immunopharmacol. 2010, 10, 331-338.
22. Karlstetter, M., Lippe, E., Walczak, Y., Moehle, C. et al., Curcumin is a potent modulator of microglial gene expression and migration. J. Neuroinflammation 2011, 8, 125.
23. Parada, E., Egea, J., Buendia, I., Negredo, P. et al., The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid. Redox Signal. 2013, 19, 1135-1148.
24. Saura, J., Tusell, J. M., Serratosa, J., High-yield isolation of murine microglia by mild trypsinization. Glia 2003, 44, 183-189.
25. Mamiya, T., Katsuoka, F., Hirayama, A., Nakajima, O. et al., Hepatocyte-specific deletion of heme oxygenase-1 disrupts redox homeostasis in basal and oxidative environments. Tohoku J. Exp. Med. 2008, 216, 331-339.
26. Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R. et al., Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8, 265-277.
27. Denizot, F., Lang, R., Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 1986, 89, 271-277.
28. Ha, H. C., Woster, P. M., Yager, J. D., Casero, R. A., Jr., The role of polyamine catabolism in polyamine analogue-induced programmed cell death. Proc. Natl. Acad. Sci. U S A 1997, 94, 11557-11562.
29. Howard, C. V., Reed, M. G., Unbiased Stereology. Three-Dimensional Measurement in Microscopy. 2nd ed. Bios Scientific Publ. 2005, Oxford, UK.
30. Rajasekar, N., Dwivedi, S., Tota, S. K., Kamat, P. K. et al., Neuroprotective effect of curcumin on okadaic acid induced memory impairment in mice. Eur. J. Pharmacol. 2013, 715, 381-394.
31. Hoppe, J. B., Haag, M., Whalley, B. J., Salbego, C. G. et al., Curcumin protects organotypic hippocampal slice cultures from Abeta1-42-induced synaptic toxicity. Toxicol. In Vitro 2013, 27, 2325-2330.
32. Kim, Y. S., Kwon, J. S., Cho, Y. K., Jeong, M. H. et al., Curcumin reduces the cardiac ischemia-reperfusion injury: involvement of the toll-like receptor 2 in cardiomyocytes. J. Nutr. Biochem. 2012, 23, 1514-1523.
33. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A. et al., Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA 2012, 109, E197-E205.
34. Liu, W., Tang, Y., Feng, J., Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci. 2011, 89, 141-146.
35. Wang, H. M., Zhao, Y. X., Zhang, S., Liu, G. D. et al., PPARgamma agonist curcumin reduces the amyloid-beta-stimulated inflammatory responses in primary astrocytes. J. Alzheimers Dis. 2010 20, 1189-1199.
36. Giulian, D., Baker, T. J., Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 1986, 6, 2163-2178.
37. Kettenmann, H., Hanisch, U. K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 2011, 91, 461-553.
38. Nemmar, A., Subramaniyan, D., Ali, B. H., Protective effect of curcumin on pulmonary and cardiovascular effects induced by repeated exposure to diesel exhaust particles in mice. PLoS One 2013, 7, e39554.
39. Zhong, F., Chen, H., Han, L., Jin, Y. et al., Curcumin attenuates lipopolysaccharide-induced renal inflammation. Biol. Pharm. Bull. 2011, 34, 226-232.
40. Guo, L., Xing, Y., Pan, R., Jiang, M. et al., Curcumin protects microglia and primary rat cortical neurons against HIV-1 gp120-mediated inflammation and apoptosis. PLoS One 2013, 8, e70565.
41. Kim, K. H., Lee, E. N., Park, J. K., Lee, J. R. et al., Curcumin attenuates TNF-alpha-induced expression of intercellular adhesion molecule-1, vascular cell adhesion molecule-1 and proinflammatory cytokines in human endometriotic stromal cells. Phytother. Res. 2012, 26, 1037-1047.
42. Gomez-Hurtado, I., Zapater, P., Bellot, P., Pascual, S. et al., Interleukin-10-mediated heme oxygenase 1-induced underlying mechanism in inflammatory down-regulation by norfloxacin in cirrhosis. Hepatology 2011, 53, 935-944.
43. Zhang, Z., Zhang, Z. Y., Wu, Y., Schluesener, H. J., Lesional accumulation of CD163+ macrophages/microglia in rat traumatic brain injury. Brain Res. 2012, 1461, 102-110.
44. Greenberg, S. S., Jie, O., Zhao, X., Wang, J. F., Role of PKC and tyrosine kinase in ethanol-mediated inhibition of LPS-inducible nitric oxide synthase. Alcohol 1998, 16, 167-175.
45. Rossol, M., Heine, H., Meusch, U., Quandt, D. et al., LPS-induced cytokine production in human monocytes and macrophages. Crit. Rev. Immunol. 2011, 31, 379-446.
46. Deshpande, R., Khalili, H., Pergolizzi, R. G., Michael, S. D. et al., Estradiol down-regulates LPS-induced cytokine production and NFkB activation in murine macrophages. Am. J. Reprod. Immunol. 1997, 38, 46-54.
47. Rangasamy, T., Guo, J., Mitzner, W. A., Roman, J. et al., Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J. Exp. Med. 2005, 202, 47-59.
48. Rangasamy, T., Cho, C. Y., Thimmulappa, R. K., Zhen, L. et al., Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 2004, 114, 1248-1259.
49. Thimmulappa, R. K., Scollick, C., Traore, K., Yates, M. et al., Nrf2-dependent protection from LPS induced inflammatory response and mortality by CDDO-Imidazolide. Biochem. Biophys. Res. Commun. 2006, 351, 883-889.
50. Chen, C., Zhang, F., Zhang, Z., Peng, M. et al., TLR4 signaling-induced heme oxygenase upregulation in the acute lung injury: role in hemorrhagic shock and two-hit induced lung inflammation. Mol. Biol. Rep. 2013, 40, 1167-1172.
51. Mandal, P., Pritchard, M. T., Nagy, L. E., Anti-inflammatory pathways and alcoholic liver disease: role of an adiponectin/interleukin-10/heme oxygenase-1 pathway. World J. Gastroenterol. 2010, 16, 1330-1336.
52. Dodd, C. A., Filipov, N. M., Manganese potentiates LPS-induced heme-oxygenase 1 in microglia but not dopaminergic cells: role in controlling microglial hydrogen peroxide and inflammatory cytokine output. Neurotoxicology 2011, 32, 683-692.
53. Wang, X. M., Kim, H. P., Nakahira, K., Ryter, S. W. et al., The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1. J. Immunol. 2009, 182, 3809-3818.
54. Godbout, J. P., Chen, J., Abraham, J., Richwine, A. F. et al., Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 2005, 19, 1329-1331.
55. Sparkman, N. L., Johnson, R. W., Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 2008, 15, 323-330.
56. Ye, S. M., Johnson, R. W., An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 2001, 9, 183-192.
57. Nolan, Y., Maher, F. O., Martin, D. S., Clarke, R. M. et al., Role of interleukin-4 in regulation of age-related inflammatory changes in the hippocampus. J. Biol. Chem. 2005, 280, 9354-9362.
58. Jayasooriya, R. G., Lee, K. T., Lee, H. J., Choi, Y. H. et al., Anti-inflammatory effects of beta-hydroxyisovalerylshikonin in BV2 microglia are mediated through suppression of the PI3K/Akt/NF-kB pathway and activation of the Nrf2/HO-1 pathway. Food Chem. Toxicol. 2014, 65, 82-89.
59. Parada, E., Egea, J., Buendia, I., Negredo, P. et al., The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid. Redox Signal. 19, 1135-1148.