Cyclooxygenases-1 and-2 differentially modulate leukocyte recruitment into the inflamed brain

Pharmacogenomics Journal

Volumn 10, Issue 5, 2010, Pages 448-457

  Choi, S H ^a   Aid, S ^a   Choi, U ^b   Bosetti, F ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

cyclooxygenase; leukocyte; LPS; neuroinflammation

Indexed keywords

CHEMOKINE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL INFILTRATION; CONTROLLED STUDY; ENCEPHALITIS; ENZYME ACTIVITY; GENE DELETION; IMMUNOMODULATION; LEUKOCYTE MIGRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BLOOD-BRAIN BARRIER; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; ENCEPHALITIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNITY, INNATE; INJECTIONS, INTRAVENTRICULAR; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS;

EID: 77957127862     PISSN: 1470269X     EISSN: 14731150     Source Type: Journal    
DOI: 10.1038/tpj.2009.68     Document Type: Article

References (70)

1. Smith WL, DeWitt DL, Garavito RM. Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 2000; 69: 145-182.
2. Bosetti F. Arachidonic acid metabolism in brain physiology and pathology: lessons from genetically altered mouse models. J Neurochem 2007; 102: 577-586.
3. Hoozemans JJ, Rozemuller JM, van Haastert ES, Veerhuis R, Eikelenboom P. Cyclooxygenase-1 and-2 in the different stages of Alzheimer's disease pathology. Curr Pharm Des 2008; 14: 1419-1427.
4. Teismann P, Tieu K, Choi DK, Wu DC, Naini A, Hunot S et al. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegen-eration. Proc Natl Acad Sci USA 2003; 100: 5473-5478.
5. Maihofner C, Probst-Cousin S, Bergmann M, Neuhuber W, Neundorfer B, Heuss D. Expression and localization of cyclooxygenase-1 and-2 in human sporadic amyotrophic lateral sclerosis. Eur J Neurosci 2003; 18: 1527-1534.
6. Murakami M, Kudo I. Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog Lipid Res 2004; 43: 3-35.
7. Aid S, Langenbach R, Bosetti F. Neuroinflammatory response to lipopolysaccharide is exacerbated in mice genetically deficient in cyclooxygenase-2. J Neuroinflammation 2008; 5: 17.
8. Choi SH, Langenbach R, Bosetti F. Genetic deletion or pharmacological inhibition of cyclooxygenase-1 attenuate lipopolysaccharide-induced inflammatory response and brain injury. FASEB J 2008; 22: 1491-1501.
9. Ubogu EE, Cossoy MB, Ransohoff RM. The expression and function of chemokines involved in CNS inflammation. Trends Pharmacol Sci 2006; 27: 48-55.
10. Shaftel SS, Griffin WS, O'Banion MK. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J Neuroinflammation 2008; 5: 7.
11. Dormond O, Bezzi M, Mariotti A, Ruegg C. Prostaglandin E2 promotes integrin alpha Vbeta 3-dependent endothelial cell adhesion, rac-activation, and spreading through cAMP/PKA-dependent signaling. J Biol Chem 2002; 277: 45838-45846.
12. Scandella E, Men Y, Legler DF, Gillessen S, Prikler L, Ludewig B et al. CCL19/CCL21-triggered signal transduction and migration of dendritic cells requires prostaglandin E2. Blood 2004; 103: 1595-1601.
13. Legler DF, Krause P, Scandella E, Singer E, Groettrup M. Prostaglandin E2 is generally required for human dendritic cell migration and exerts its effect via EP2 and EP4 receptors. J Immunol 2006; 176: 966-973.
14. Weller CL, Collington SJ, Hartnell A, Conroy DM, Kaise T, Barker JE et al. Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proc Natl Acad Sci USA 2007; 104: 11712-11717.
15. Tajima T, Murata T, Aritake K, Urade Y, Hirai H, Nakamura M et al. Lipopolysaccharide induces macrophage migration via prostaglandin D(2) and prostaglandin E(2). J Pharmacol Exp Ther 2008; 326: 493-501.
16. Schmidley JW, Dadson J, Iyer RS, Salomon RG. Brain tissue injury and blood-brain barrier opening induced by injection of LGE2 or PGE2. Prostaglandins Leukot Essent Fatty Acids 1992; 47: 105-110.
17. Tuomanen E, Hengstler B, Rich R, Bray MA, Zak O, Tomasz A. Nonsteroidal anti-inflammatory agents in the therapy for experimental pneumococcal meningitis. J Infect Dis 1987; 155: 985-990.
18. Kadurugamuwa JL, Hengstler B, Zak O. Cerebrospinal fluid protein profile in experimental pneumococcal meningitis and its alteration by ampicillin and anti-inflammatory agents. J Infect Dis 1989; 159: 26-34.
19. Candelario-Jalil E, Taheri S, Yang Y, Sood R, Grossetete M, Estrada EY et al. Cyclooxygenase inhibition limits blood-brain barrier disruption following intracerebral injection of tumor necrosis factor-alpha in the rat. J Pharmacol Exp Ther 2007; 323: 488-498.
20. Issekutz AC, Bhimji S. The effect of nonsteroidal anti-inflammatory agents on E. coli-induced inflammation. Immunopharmacology 1982; 4: 11-22.
21. Shimanuki T, Nakamura RM, diZerega GS. In vivo modulation of leukotaxis by non-steroidal anti-inflammatory drugs. Agents Actions 1985; 17: 80-83.
22. Hirasawa N, Ohuchi K, Watanabe M, Tsurufuji S. Mechanism of the inhibitory action of cyclooxygenase inhibitors on leukocyte infiltration: involvement of endogenous histamine. Eur J Pharmacol 1987; 144: 267-275.
23. Montine TJ, Milatovic D, Gupta RC, Valyi-Nagy T, Morrow JD, Breyer RM. Neuronal oxidative damage from activated innate immunity is EP2 receptor-dependent. J Neurochem 2002; 83: 463-470.
24. Bonow RH, Aid S, Zhang Y, Becker KG, Bosetti F. The brain expression of genes involved in inflammatory response, the ribosome, and learning and memory is altered by centrally injected lipopolysaccharide in mice. Pharmacogenomics J 2009; 9: 116-126.
25. Langenbach R, Morham SG, Tiano HF, Loftin CD, Ghanayem BI, Chulada PC et al. Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 1995; 83: 483-492.
26. Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC et al. Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 1995; 83: 473-482.
27. Delgado M, Ganea D. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J 2003; 17: 1922-1924.
28. Milatovic D, Zaja-Milatovic S, Montine KS, Shie FS, Montine TJ. Neuronal oxidative damage and dendritic degeneration following activation of CD14-dependent innate immune response in vivo. J Neuroinflammation 2004; 1: 20.
29. Gao HM, Kotzbauer PT, Uryu K, Leight S, Trojanowski JQ, Lee VM. Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. J Neurosci 2008; 28: 7687-7698.
30. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego, CA, 2001, xxv, 264pp.
31. McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1-and neutrophil-dependent mechanisms. J Neurosci 2007; 27: 4403-4412.
32. Kinoshita K, Kraydieh S, Alonso O, Hayashi N, Dietrich WD. Effect of posttraumatic hyperglycemia on contusion volume and neutrophil accumulation after moderate fluid-percussion brain injury in rats. J Neurotrauma 2002; 19: 681-692.
33. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C et al. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 2007; 13: 432-438.
34. Babcock AA, Kuziel WA, Rivest S, Owens T. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 2003; 23: 7922-7930.
35. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. Mature microglia resemble immature antigen-presenting cells. Glia 1998; 22: 72-85.
36. Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA 1991; 88: 7438-7442.
37. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 1995; 154: 4309-4321.
38. Lagasse E, Weissman IL. Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods 1996; 197: 139-150.
39. D'Mello C, Le T, Swain MG. Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J Neurosci 2009; 29: 2089-2102.
40. Blamire AM, Anthony DC, Rajagopalan B, Sibson NR, Perry VH, Styles P. Interleukin-1beta-induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J Neurosci 2000; 20: 8153-8159.
41. Hao Q, Chen Y, Zhu Y, Fan Y, Palmer D, Su H et al. Neutrophil depletion decreases VEGF-induced focal angiogenesis in the mature mouse brain. J Cereb Blood Flow Metab 2007; 27: 1853-1860.
42. Eliason JL, Hannawa KK, Ailawadi G, Sinha I, Ford JW, Deogracias MP et al. Neutrophil depletion inhibits experimental abdominal aortic aneurysm formation. Circulation 2005; 112: 232-240.
43. Choi DK, Pennathur S, Perier C, Tieu K, Teismann P, Wu DC et al. Ablation of the inflammatory enzyme myeloperoxidase mitigates features of Parkinson's disease in mice. J Neurosci 2005; 25: 6594-6600.
44. Shaftel SS, Carlson TJ, Olschowka JA, Kyrkanides S, Matousek SB, O'Banion MK. Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J Neurosci 2007; 27: 9301-9309.
45. Ransohoff RM, Kivisakk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003; 3: 569-581.
46. Floris S, Blezer EL, Schreibelt G, Dopp E, van der Pol SM, Schadee-Eestermans IL et al. Blood-brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: a quantitative MRI study. Brain 2004; 127: 616-627.
47. Savarin-Vuaillat C, Ransohoff RM. Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce? Neurotherapeutics 2007; 4: 590-601.
48. Choi SH, Aid S, Bosetti F. The distinct roles of cyclooxygenase-1 and-2 in neuroinflammation: implications for translational research. Trends Pharmacol Sci 2009; 30: 174-181.
49. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10: 1387-1394.
50. Justicia C, Panes J, Sole S, Cervera A, Deulofeu R, Chamorro A et al. Neutrophil infiltration increases matrix metalloproteinase-9 in the ischemic brain after occlusion/reperfusion of the middle cerebral artery in rats. J Cereb Blood Flow Metab 2003; 23: 1430-1440.
51. Kantari C, Pederzoli-Ribeil M, Witko-Sarsat V. The role of neutrophils and monocytes in innate immunity. Contrib Microbiol 2008; 15: 118-146.
52. Lau D, Mollnau H, Eiserich JP, Freeman BA, Daiber A, Gehling UM et al. Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc Natl Acad Sci USA 2005; 102: 431-436.
53. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunol Rev 2000; 177: 195-203.
54. Wang PY, Kao CH, Mui MY, Wang SJ. Leukocyte infiltration in acute hemispheric ischemic stroke. Stroke 1993; 24: 236-240.
55. McGeer EG, McGeer PL. Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27: 741-749.
56. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest 2009; 119: 182-192.
57. Akopov SE, Simonian NA, Grigorian GS. Dynamics of poly-morphonuclear leukocyte accumulation in acute cerebral infarction and their correlation with brain tissue damage. Stroke 1996; 27: 1739-1743.
58. Price CJ, Menon DK, Peters AM, Ballinger JR, Barber RW, Balan KK et al. Cerebral neutrophil recruitment, histology, and outcome in acute ischemic stroke: an imaging-based study. Stroke 2004; 35: 1659-1664.
59. Gidday JM, Gasche YG, Copin JC, Shah AR, Perez RS, Shapiro SD et al. Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am J Physiol Heart Circ Physiol 2005; 289: H558-H568.
60. Ryu JK, Tran KC, McLarnon JG. Depletion of neutrophils reduces neuronal degeneration and inflammatory responses induced by quinolinic acid in vivo. Glia 2007; 55: 439-451.
61. Choi SH, Bosetti F. Cyclooxygenase-1 null mice show reduced neuroinflammation in response to b-amyloid. Aging 2009; 1: 234-244.
62. Aid S, Bosetti F. Gene expression of cyclooxygenase-1 and Ca(2+)-independent phospholipase A(2) is altered in rat hippocampus during normal aging. Brain Res Bull 2007; 73: 108-113.
63. Serhan CN, Chiang N. Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus. Br J Pharmacol 2008; 153(Suppl 1): S200-S215.
64. Blais V, Turrin NP, Rivest S. Cyclooxygenase 2 (COX-2) inhibition increases the inflammatory response in the brain during systemic immune stimuli. J Neurochem 2005; 95: 1563-1574.
65. Iadecola C, Niwa K, Nogawa S, Zhao X, Nagayama M, Araki E et al. Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc Natl Acad Sci USA 2001; 98: 1294-1299.
66. Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Alvarez D, Al-Dalain S, Martinez G et al. Assessment of the relative contribution of COX-1 and COX-2 isoforms to ischemia-induced oxidative damage and neurodegeneration following transient global cerebral ischemia. J Neurochem 2003; 86: 545-555.
67. Sasaki T, Kitagawa K, Yamagata K, Takemiya T, Tanaka S, Omura-Matsuoka E et al. Amelioration of hippocampal neuronal damage after transient forebrain ischemia in cyclooxygenase-2-deficient mice. J Cereb Blood Flow Metab 2004; 24: 107-113.
68. Poligone B, Baldwin AS. Positive and negative regulation of NF-kappaB by COX-2: roles of different prostaglandins. J Biol Chem 2001; 276: 38658-38664.
69. Yen JH, Khayrullina T, Ganea D. PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood 2008; 111: 260-270.
70. Pavlovic S, Du B, Sakamoto K, Khan KM, Natarajan C, Breyer RM et al. Targeting prostaglandin E2 receptors as an alternative strategy to block cyclooxygenase-2-dependent extracellular matrix-induced matrix me-talloproteinase-9 expression by macrophages. J Biol Chem 2006; 281: 3321-3328.