Nuclear factor-κB activation regulates cyclooxygenase-2 induction in human astrocytes in response to CXCL12: Role in neuronal toxicity

Journal of Neurochemistry

Volumn 113, Issue 3, 2010, Pages 772-783

  Álvarez, Susana ^a   Blanco, Almudena ^b   Fresno, Manuel ^a,c   Muñoz Fernández, Moángeles ^b,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^c CSIC   (Spain)

Author keywords

Brain; Inflammation; Neurotoxicity

Indexed keywords

CHEMOKINE; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROSTAGLANDIN E2; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR RELA; CXCL12 PROTEIN, HUMAN; LUCIFERASE; MESSENGER RNA;

ARTICLE; ASTROCYTE; CELL VIABILITY; CONTROLLED STUDY; ENZYME REGULATION; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; NERVE DEGENERATION; NEUROBLASTOMA CELL; NEUROTOXICITY; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSCRIPTION INITIATION; BIOSYNTHESIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECT; ENZYME INDUCTION; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PLASMID; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ASTROCYTES; BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHEMOKINE CXCL12; CYCLOOXYGENASE 2; DINOPROSTONE; ENZYME INDUCTION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LUCIFERASES; NEURONS; NF-KAPPA B; PLASMIDS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 77950630894     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06646.x     Document Type: Article

References (75)

1. Ahmad A. S., Ahmad M., de Brum-Fernandes A. J. Dore S. (2005) Prostaglandin EP4 receptor agonist protects against acute neurotoxicity. Brain Res. 1066, 71 77.
2. Aid S., Langenbach R. Bosetti F. (2008) Neuroinflammatory response to lipopolysaccharide is exacerbated in mice genetically deficient in cyclooxygenase-2. J. Neuroinflammation 5, 17.
3. Alvarez S., Serramia M. J., Fresno M. Munoz-Fernandez M. (2005) Human immunodeficiency virus type 1 envelope glycoprotein 120 induces cyclooxygenase-2 expression in neuroblastoma cells through a nuclear factor-kappaB and activating protein-1 mediated mechanism. J. Neurochem. 94, 850 861.
4. Alvarez S., Serramia M. J., Fresno M. Munoz-Fernandez M. A. (2007) HIV-1 envelope glycoprotein 120 induces cyclooxygenase-2 expression in astrocytoma cells through a nuclear factor-kappaB-dependent mechanism. Neuromolecular Med. 9, 179 193.
5. Bajetto A., Barbero S., Bonavia R., Piccioli P., Pirani P., Florio T. Schettini G. (2001) Stromal cell-derived factor-1alpha induces astrocyte proliferation through the activation of extracellular signal-regulated kinases 1/2 pathway. J. Neurochem. 77, 1226 1236.
6. Bertolini A., Ottani A. Sandrini M. (2002) Selective COX-2 inhibitors and dual acting anti-inflammatory drugs: critical remarks. Curr. Med. Chem. 9, 1033 1043.
7. Bezzi P. Volterra A. (2001) A neuron-glia signalling network in the active brain. Curr. Opin. Neurobiol. 11, 387 394.
8. Bezzi P., Domercq M., Brambilla L. et al. (2001) CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4, 702 710.
9. Blanco A., Alvarez S., Fresno M. Munoz-Fernandez M. A. (2008) Extracellular HIV-Tat induces cyclooxygenase-2 in glial cells through activation of nuclear factor of activated T cells. J. Immunol. 180, 530 540.
10. Bleul C. C., Farzan M., Choe H., Parolin C., Clark-Lewis I., Sodroski J. Springer T. A. (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV entry. Nature 382, 829 833.
11. Bonavia R., Bajetto A., Barbero S., Pirani P., Florio T. Schettini G. (2003) Chemokines and their receptors in the CNS: expression of CXCL12/SDF-1 and CXCR4 and their role in astrocyte proliferation. Toxicol. Lett. 139, 181 189.
12. Burns J. M., Summers B. C., Wang Y. et al. (2006) A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 203, 2201 2213.
13. Candelario-Jalil E., de Oliveira A. C., Graf S., Bhatia H. S., Hull M., Munoz E. Fiebich B. L. (2007) Resveratrol potently reduces prostaglandin E2 production and free radical formation in lipopolysaccharide-activated primary rat microglia. J. Neuroinflammation 4, 25.
14. Carlson N. G., Hill K. E., Tsunoda I., Fujinami R. S. Rose J. W. (2006) The pathologic role for COX-2 in apoptotic oligodendrocytes in virus induced demyelinating disease: implications for multiple sclerosis. J. Neuroimmunol. 174, 21 31.
15. Carrasco E., Casper D. Werner P. (2007) PGE(2) receptor EP1 renders dopaminergic neurons selectively vulnerable to low-level oxidative stress and direct PGE(2) neurotoxicity. J. Neurosci. Res. 85, 3109 3117.
16. Chandrasekharan N. V., Dai H., Roos K. L., Evanson N. K., Tomsik J., Elton T. S. Simmons D. L. (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc. Natl Acad. Sci. USA 99, 13926 13931.
17. Choi S. H., Langenbach R. Bosetti F. (2008) Genetic deletion or pharmacological inhibition of cyclooxygenase-1 attenuate lipopolysaccharide- induced inflammatory response and brain injury. FASEB J. 22, 1491 1501.
18. Chu C. Y., Cha S. T., Lin W. C., Lu P. H., Tan C. T., Chang C. C., Lin B. R., Jee S. H. Kuo M. L. (2009) Stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12)-enhanced angiogenesis of human basal cell carcinoma cells involves ERK1/2-NF-kappaB/interleukin-6 pathway. Carcinogenesis 30, 205 213.
19. Chun K. S. Surh Y. J. (2004) Signal transduction pathways regulating cyclooxygenase-2 expression: potential molecular targets for chemoprevention. Biochem. Pharmacol. 68, 1089 1100.
20. Domoki F., Perciaccante J. V., Puskar M., Bari F. Busija D. W. (2001) Cyclooxygenase-2 inhibitor NS398 preserves neuronal function after hypoxia/ischemia in piglets. Neuroreport 12, 4065 4068.
21. Echeverria V., Clerman A. Dore S. (2005) Stimulation of PGE receptors EP2 and EP4 protects cultured neurons against oxidative stress and cell death following beta-amyloid exposure. Eur. J. Neurosci. 22, 2199 2206.
22. Fernandis A. Z., Prasad A., Band H., Klosel R. Ganju R. K. (2004) Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 23, 157 167.
23. Ghosh S., May M. J. Kopp E. B. (1998) NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225 260.
24. Ghoshal A., Das S., Ghosh S., Mishra M. K., Sharma V., Koli P., Sen E. Basu A. (2007) Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55, 483 496.
25. Gleichmann M., Gillen C., Czardybon M., Bosse F., Greiner-Petter R., Auer J. Muller H. W. (2000) Cloning and characterization of SDF-1gamma, a novel SDF-1 chemokine transcript with developmentally regulated expression in the nervous system. Eur. J. Neurosci. 12, 1857 1866.
26. Gorgoni B., Caivano M., Arizmendi C. Poli V. (2001) The transcription factor C/EBPbeta is essential for inducible expression of the cox-2 gene in macrophages but not in fibroblasts. J. Biol. Chem. 276, 40769 40777.
27. Han Y., He T., Huang D. R., Pardo C. A. Ransohoff R. M. (2001) TNF-alpha mediates SDF-1 alpha-induced NF-kappa B activation and cytotoxic effects in primary astrocytes. J. Clin. Invest. 108, 425 435.
28. Hou C. H., Tan T. W. Tang C. H. (2008) AMP-activated protein kinase is involved in COX-2 expression in response to ultrasound in cultured osteoblasts. Cell. Signal. 20, 978 988.
29. Hsieh H. L., Wang H. H., Wu C. Y., Jou M. J., Yen M. H., Parker P. Yang C. M. (2007) BK-induced COX-2 expression via PKC-delta-dependent activation of p42/p44 MAPK and NF-kappaB in astrocytes. Cell. Signal. 19, 330 340.
30. Iadecola C., Niwa K., Nogawa S., Zhao X., Nagayama M., Araki E., Morham S. Ross M. E. (2001) Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc. Natl Acad. Sci. USA 98, 1294 1299.
31. Iniguez M. A., Martinez-Martinez S., Punzon C., Redondo J. M. Fresno M. (2000) An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J. Biol. Chem. 275, 23627 23635.
32. Inoue H. Tanabe T. (1998) Transcriptional role of the nuclear factor kappa B site in the induction by lipopolysaccharide and suppression by dexamethasone of cyclooxygenase-2 in U937 cells. Biochem. Biophys. Res. Commun. 244, 143 148.
33. Inoue H., Yokoyama C., Hara S., Tone Y. Tanabe T. (1995) Transcriptional regulation of human prostaglandin-endoperoxide synthase-2 gene by lipopolysaccharide and phorbol ester in vascular endothelial cells. Involvement of both nuclear factor for interleukin-6 expression site and cAMP response element. J. Biol. Chem. 270, 24965 24971.
34. Ishige K., Chen Q., Sagara Y. Schubert D. (2001) The activation of dopamine D4 receptors inhibits oxidative stress-induced nerve cell death. J. Neurosci. 21, 6069 6076.
35. Karin M., Cao Y., Greten F. R. Li Z. W. (2002) NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2, 301 310.
36. Kauffman G. L. (1997) Stress, the brain, and the gastric mucosa. Am. J. Surg. 174, 271 275.
37. Kawano T., Anrather J., Zhou P., Park L., Wang G., Frys K. A., Kunz A., Cho S., Orio M. Iadecola C. (2006) Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat. Med. 12, 225 229.
38. Klein R. S. Rubin J. B. (2004) Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity. Trends Immunol. 25, 306 314.
39. Koller H., Siebler M. Hartung H. P. (1997) Immunologically induced electrophysiological dysfunction: implications for inflammatory diseases of the CNS and PNS. Prog. Neurobiol. 52, 1 26.
40. Kukreja P., Abdel-Mageed A. B., Mondal D., Liu K. Agrawal K. C. (2005) Up-regulation of CXCR4 expression in PC-3 cells by stromal-derived factor-1alpha (CXCL12) increases endothelial adhesion and transendothelial migration: role of MEK/ERK signaling pathway-dependent NF-kappaB activation. Cancer Res. 65, 9891 9898.
41. Li M. Ransohoff R. M. (2008) Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 84, 116 131.
42. Li J., Liang X., Wang Q., Breyer R. M., McCullough L. Andreasson K. (2008) Misoprostol, an anti-ulcer agent and PGE(2) receptor agonist, protects against cerebral ischemia. Neurosci. Lett. 438, 210 215.
43. Lu M., Grove E. A. Miller R. J. (2002) Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl Acad. Sci. USA 99, 7090 7095.
44. Lucas S. M., Rothwell N. J. Gibson R. M. (2006) The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 147 (Suppl. 1 S232 S240.
45. Madrigal J. L., Garcia-Bueno B., Caso J. R., Perez-Nievas B. G. Leza J. C. (2006) Stress-induced oxidative changes in brain. CNS Neurol. Disord. Drug Targets 5, 561 568.
46. Massa A., Casagrande S., Bajetto A. et al. (2006) SDF-1 controls pituitary cell proliferation through the activation of ERK1/2 and the Ca2+-dependent, cytosolic tyrosine kinase Pyk2. Ann. N Y Acad. Sci. 1090, 385 398.
47. McGrath K. E., Koniski A. D., Maltby K. M., McGann J. K. Palis J. (1999) Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 213, 442 456.
48. Metelitsa L. S., Wu H. W., Wang H., Yang Y., Warsi Z., Asgharzadeh S., Groshen S., Wilson S. B. Seeger R. C. (2004) Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J. Exp. Med. 199, 1213 1221.
49. Morris J. K. Richards J. S. (1996) An E-box region within the prostaglandin endoperoxide synthase-2 (PGS-2) promoter is required for transcription in rat ovarian granulosa cells. J. Biol. Chem. 271, 16633 16643.
50. Nagasawa T., Kikutani H. Kishimoto T. (1994) Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc. Natl Acad. Sci. USA 91, 2305 2309.
51. Nie M., Pang L., Inoue H. Knox A. J. (2003) Transcriptional regulation of cyclooxygenase 2 by bradykinin and interleukin-1beta in human airway smooth muscle cells: involvement of different promoter elements, transcription factors, and histone h4 acetylation. Mol. Cell. Biol. 23, 9233 9244.
52. Niwa K., Araki E., Morham S. G., Ross M. E. Iadecola C. (2000) Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J. Neurosci. 20, 763 770.
53. Nogawa S., Zhang F., Ross M. E. Iadecola C. (1997) Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci. 17, 2746 2755.
54. Odemis V., Moepps B., Gierschik P. Engele J. (2002) Interleukin-6 and cAMP induce stromal cell-derived factor-1 chemotaxis in astroglia by up-regulating CXCR4 cell surface expression. Implications for brain inflammation. J. Biol. Chem. 277, 39801 39808.
55. Peng H., Erdmann N., Whitney N., Dou H., Gorantla S., Gendelman H. E., Ghorpade A. Zheng J. (2006) HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 54, 619 629.
56. Pepicelli O., Fedele E., Berardi M., Raiteri M., Levi G., Greco A., Ajmone-Cat M. A. Minghetti L. (2005) Cyclo-oxygenase-1 and -2 differently contribute to prostaglandin E2 synthesis and lipid peroxidation after in vivo activation of N-methyl-d-aspartate receptors in rat hippocampus. J. Neurochem. 93, 1561 1567.
57. Rollins B. J. (1997) Chemokines. Blood 90, 909 928.
58. Rosenkilde M. M., Gerlach L. O., Jakobsen J. S., Skerlj R. T., Bridger G. J. Schwartz T. W. (2004) Molecular mechanism of AMD3100 antagonism in the CXCR4 receptor: transfer of binding site to the CXCR3 receptor. J. Biol. Chem. 279, 3033 3041.
59. Rostasy K., Egles C., Chauhan A., Kneissl M., Bahrani P., Yiannoutsos C., Hunter D. D., Nath A., Hedreen J. C. Navia B. A. (2003) SDF-1alpha is expressed in astrocytes and neurons in the AIDS dementia complex: an in vivo and in vitro study. J. Neuropathol. Exp. Neurol. 62, 617 626.
60. Salcedo R. Oppenheim J. J. (2003) Role of chemokines in angiogenesis: CXCL12/SDF-1 and CXCR4 interaction, a key regulator of endothelial cell responses. Microcirculation 10, 359 370.
61. Shirozu M., Nakano T., Inazawa J., Tashiro K., Tada H., Shinohara T. Honjo T. (1995) Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 28, 495 500.
62. Stumm R. K., Rummel J., Junker V., Culmsee C., Pfeiffer M., Krieglstein J., Hollt V. Schulz S. (2002) A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J. Neurosci. 22, 5865 5878.
63. Su C. M., Lu D. Y., Hsu C. J. et al. (2009) Glial cell-derived neurotrophic factor increases migration of human chondrosarcoma cells via ERK and NF-kappaB pathways. J. Cell. Physiol. 220, 499 507.
64. Tabatabai G., Frank B., Mohle R., Weller M. Wick W. (2006) Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain 129, 2426 2435.
65. Tazawa R., Xu X. M., Wu K. K. Wang L. H. (1994) Characterization of the genomic structure, chromosomal location and promoter of human prostaglandin H synthase-2 gene. Biochem. Biophys. Res. Commun. 203, 190 199.
66. Toscano C. D., Ueda Y., Tomita Y. A., Vicini S. Bosetti F. (2008) Altered GABAergic neurotransmission is associated with increased kainate-induced seizure in prostaglandin-endoperoxide synthase-2 deficient mice. Brain Res. Bull. 75, 598 609.
67. Vesce S., Rossi D., Brambilla L. Volterra A. (2007) Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int. Rev. Neurobiol. 82, 57 71.
68. Vijitruth R., Liu M., Choi D. Y., Nguyen X. V., Hunter R. L. Bing G. (2006) Cyclooxygenase-2 mediates microglial activation and secondary dopaminergic cell death in the mouse MPTP model of Parkinson's disease. J. Neuroinflammation 3, 6.
69. Vila-Coro A. J., Rodriguez-Frade J. M., Martin De Ana A., Moreno-Ortiz M. C., Martinez A. C. Mellado M. (1999) The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. 13, 1699 1710.
70. Volterra A. Meldolesi J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626 640.
71. Wu W., Silbajoris R. A., Whang Y. E., Graves L. M., Bromberg P. A. Samet J. M. (2005) p38 and EGF receptor kinase-mediated activation of the phosphatidylinositol 3-kinase/Akt pathway is required for Zn2 + -induced cyclooxygenase-2 expression. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L883 L889.
72. Xie W., Fletcher B. S., Andersen R. D. Herschman H. R. (1994) v-src induction of the TIS10/PGS2 prostaglandin synthase gene is mediated by an ATF/CRE transcription response element. Mol. Cell. Biol. 14, 6531 6539.
73. Yamagata K., Andreasson K. I., Kaufmann W. E., Barnes C. A. Worley P. F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11, 371 386.
74. Yang H. Chen C. (2008) Cyclooxygenase-2 in synaptic signaling. Curr. Pharm. Des. 14, 1443 1451.
75. Yokoyama C. Tanabe T. (1989) Cloning of human gene encoding prostaglandin endoperoxide synthase and primary structure of the enzyme. Biochem. Biophys. Res. Commun. 165, 888 894.