Ceruloplasmin potentiates nitric oxide synthase activity and cytokine secretion in activated microglia

Journal of Neuroinflammation

Volumn 11, Issue 1, 2014, Pages

  Lazzaro, Massimo ^a   Bettegazzi, Barbara ^a   Barbariga, Marco ^a   Codazzi, Franca ^a   Zacchetti, Daniele ^a   Alessio, Massimo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Ceruloplasmin; Inducible nitric oxide synthase; Lipopolysaccharide; Microglial cells; Neuroinflammation

Indexed keywords

CERULOPLASMIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; CYTOKINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; MICROGLIA; NERVE CELL CULTURE; NONHUMAN; OXIDATION; PRIMARY CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; HUMAN; INFLAMMATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ANIMALS; BLOTTING, WESTERN; CERULOPLASMIN; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INFLAMMATION; MICROGLIA; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84910058865     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0164-9     Document Type: Article

References (67)

1. Hellman NE, Gitlin JD. Ceruloplasmin metabolism and function. Annu Rev Nutr 2002, 22:439-458. 10.1146/annurev.nutr.22.012502.114457, 12055353.
2. Patel BN, David S. A novel glycosylphosphatidylinositol-anchored form of ceruloplasmin is expressed by mammalian astrocytes. J Biol Chem 1997, 272:20185-20190. 10.1074/jbc.272.32.20185, 9242695.
3. Mittal B, Doroudchi MM, Jeong SY, Patel BN, David S. Expression of a membrane-bound form of the ferroxidase ceruloplasmin by leptomeningeal cells. Glia 2003, 41:337-346. 10.1002/glia.10158, 12555201.
4. Duce JA, Tsatsanis A, Cater MA, James SA, Robb E, Wikhe K, Leong SL, Perez K, Johanssen T, Greenough MA, Cho HH, Galatis D, Moir RD, Masters CL, McLean C, Tanzi RE, Cappai R, Barnham KJ, Ciccotosto GD, Rogers JT, Bush AI. Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 2010, 142:857-867. 10.1016/j.cell.2010.08.014, 20817278.
5. Jeong SY, David S. Glycosylphosphatidylinositol-anchored ceruloplasmin is required for iron efflux from cells in the central nervous system. J Biol Chem 2003, 278:27144-27148. 10.1074/jbc.M301988200, 12743117.
6. Olivieri S, Conti A, Iannaccone S, Cannistraci CV, Campanella A, Barbariga M, Codazzi F, Pelizzoni I, Magnani G, Pesca M, Franciotta D, Cappa SF, Alessio M. Ceruloplasmin oxidation, a feature of Parkinson's disease CSF, inhibits ferroxidase activity and promotes cellular iron retention. J Neurosci 2011, 31:18568-18577. 10.1523/JNEUROSCI.3768-11.2011, 22171055.
7. Grimm S, Hoehn A, Davies KJ, Grune T. Protein oxidative modifications in the ageing brain: consequence for the onset of neurodegenerative disease. Free Radic Res 2011, 45:73-88. 10.3109/10715762.2010.512040, 20815785.
8. Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR. Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 2004, 5:863-873. 10.1038/nrn1537, 15496864.
9. Corti A, Curnis F. Isoaspartate-dependent molecular switches for integrin-ligand recognition. J Cell Sci 2011, 124:515-522. 10.1242/jcs.077172, 21282473.
10. Barbariga M, Curnis F, Spitaleri A, Andolfo A, Zucchelli C, Lazzaro M, Magnani G, Musco G, Corti A, Alessio M. Oxidation-induced structural changes of ceruloplasmin foster NGR-motifs deamidation that promote integrin binding and signalling. J Biol Chem 2014, 289:3736-3748. 10.1074/jbc.M113.520981, 24366863.
11. Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 2011, 11:775-787. 10.1038/nri3086, 22025055.
12. Graeber MB, Streit WJ. Microglia: biology and pathology. Acta Neuropathol 2010, 119:89-105. 10.1007/s00401-009-0622-0, 20012873.
13. Graeber MB, Li W, Rodriguez ML. Role of microglia in CNS inflammation. FEBS Lett 2011, 585:3798-3805. 10.1016/j.febslet.2011.08.033, 21889505.
14. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, et al. Inflammation and Alzheimer's disease. Neurobiol Aging 2000, 21:383-421. 10.1016/S0197-4580(00)00124-X, 10858586.
15. Cameron B, Landreth GE. Inflammation, microglia, and Alzheimer's disease. Neurobiol Dis 2010, 37:503-509. 10.1016/j.nbd.2009.10.006, 19833208.
16. Teismann P, Tieu K, Cohen O, Choi DK, Wu DC, Marks D, Vila M, Jackson-Lewis V, Przedborski S. Pathogenic role of glial cells in Parkinson's disease. Mov Disord 2003, 18:121-129. 10.1002/mds.10332, 12539204.
17. Tufekci KU, Meuwissen R, Genc S, Genc K. Inflammation in Parkinson's disease. Adv Protein Chem Struct Biol 2012, 88:69-132. 10.1016/B978-0-12-398314-5.00004-0, 22814707.
18. Perry VH. Innate inflammation in Parkinson's disease. Cold Spring Harb Perspect Med 2012, 2:a009373. 10.1101/cshperspect.a009373, 22951445.
19. Peterson LJ, Flood PM. Oxidative stress and microglial cells in Parkinson's disease. Mediators Inflamm 2012, 2012:401264. 10.1155/2012/401264, 22544998.
20. Ricci S, Fuso A, Ippoliti F, Businaro R. Stress-induced cytokines and neuronal dysfunction in Alzheimer's disease. J Alzheimers Dis 2012, 28:11-24. 22124029.
21. Swardfager W, Lanctot K, Rothenburg L, Wong A, Cappell J, Herrmann N. A meta-analysis of cytokines in Alzheimer's disease. Biol Psychiatry 2010, 68:930-941. 10.1016/j.biopsych.2010.06.012, 20692646.
22. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934. 10.1016/j.cell.2010.02.016, 20303880.
23. Cunningham C. Microglia and neurodegeneration: the role of systemic inflammation. Glia 2013, 61:71-90. 10.1002/glia.22350, 22674585.
24. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 2003, 100:8514-8519. 10.1073/pnas.1432609100, 12824464.
25. Beraud D, Hathaway HA, Trecki J, Chasovskikh S, Johnson DA, Johnson JA, Federoff HJ, Shimoji M, Mhyre TR, Maguire-Zeiss KA. Microglial activation and antioxidant responses induced by the Parkinson's disease protein alpha-synuclein. J Neuroimmune Pharmacol 2013, 8:94-117. 10.1007/s11481-012-9401-0, 23054368.
26. Sondag CM, Dhawan G, Combs CK. Beta amyloid oligomers and fibrils stimulate differential activation of primary microglia. J Neuroinflammation 2009, 6:1. 10.1186/1742-2094-6-1, 19123954.
27. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007, 8:57-69. 10.1038/nrn2038, 17180163.
28. Gabellec MM, Griffais R, Fillion G, Haour F. Expression of interleukin 1 alpha, interleukin 1 beta and interleukin 1 receptor antagonist mRNA in mouse brain: regulation by bacterial lipopolysaccharide (LPS) treatment. Brain Res Mol Brain Res 1995, 31:122-130. 10.1016/0169-328X(95)00042-Q, 7476020.
29. Turrin NP, Gayle D, Ilyin SE, Flynn MC, Langhans W, Schwartz GJ, Plata-Salaman CR. Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res Bull 2001, 54:443-453. 10.1016/S0361-9230(01)00445-2, 11306198.
30. Quan N, He L, Lai W. Endothelial activation is an intermediate step for peripheral lipopolysaccharide induced activation of paraventricular nucleus. Brain Res Bull 2003, 59:447-452. 10.1016/S0361-9230(02)00951-6, 12576141.
31. Singh AK, Jiang Y. How does peripheral lipopolysaccharide induce gene expression in the brain of rats?. Toxicology 2004, 201:197-207. 10.1016/j.tox.2004.04.015, 15297033.
32. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 2005, 25:9275-9284. 10.1523/JNEUROSCI.2614-05.2005, 16207887.
33. Saper CB. The dance of the perivascular and endothelial cells: mechanisms of brain response to immune signaling. Neuron 2010, 65:4-6. 10.1016/j.neuron.2009.12.029, 20152108.
34. Raivich G, Bohatschek M, Werner A, Jones LL, Galiano M, Kloss CU, Zhu XZ, Pfeffer K, Liu ZQ. Lymphocyte infiltration in the injured brain: role of proinflammatory cytokines. J Neurosci Res 2003, 72:726-733. 10.1002/jnr.10621, 12774313.
35. Dutta G, Zhang P, Liu B. The lipopolysaccharide Parkinson's disease animal model: mechanistic studies and drug discovery. Fundam Clin Pharmacol 2008, 22:453-464. 10.1111/j.1472-8206.2008.00616.x, 18710400.
36. Erickson MA, Hartvigson PE, Morofuji Y, Owen JB, Butterfield DA, Banks WA. Lipopolysaccharide impairs amyloid beta efflux from brain: altered vascular sequestration, cerebrospinal fluid reabsorption, peripheral clearance and transporter function at the blood-brain barrier. J Neuroinflammation 2012, 9:150. 10.1186/1742-2094-9-150, 22747709.
37. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B. Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 2002, 81:1285-1297. 10.1046/j.1471-4159.2002.00928.x, 12068076.
38. Jaeger LB, Dohgu S, Sultana R, Lynch JL, Owen JB, Erickson MA, Shah GN, Price TO, Fleegal-Demotta MA, Butterfield DA, Banks WA. Lipopolysaccharide alters the blood-brain barrier transport of amyloid beta protein: a mechanism for inflammation in the progression of Alzheimer's disease. Brain Behav Immun 2009, 23:507-517. 10.1016/j.bbi.2009.01.017, 19486646.
39. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462. 10.1002/glia.20467, 17203472.
40. Lee KH, Yun SJ, Nam KN, Gho YS, Lee EH. Activation of microglial cells by ceruloplasmin. Brain Res 2007, 1171:1-8. 10.1016/j.brainres.2007.07.053, 17727827.
41. Consonni A, Morara S, Codazzi F, Grohovaz F, Zacchetti D. Inhibition of lipopolysaccharide-induced microglia activation by calcitonin gene related peptide and adrenomedullin. Mol Cell Neurosci 2011, 48:151-160. 10.1016/j.mcn.2011.07.006, 21803157.
42. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980, 85:890-902. 10.1083/jcb.85.3.890, 6248568.
43. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011, 91:461-553. 10.1152/physrev.00011.2010, 21527731.
44. Macco R, Pelizzoni I, Consonni A, Vitali I, Giacalone G, Martinelli Boneschi F, Codazzi F, Grohovaz F, Zacchetti D. Astrocytes acquire resistance to iron-dependent oxidative stress upon proinflammatory activation. J Neuroinflammation 2013, 10:130. 10.1186/1742-2094-10-130, 24160637.
45. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982, 126:131-138. 10.1016/0003-2697(82)90118-X, 7181105.
46. Sheng W, Zong Y, Mohammad A, Ajit D, Cui J, Han D, Hamilton JL, Simonyi A, Sun AY, Gu Z, Hong JS, Weisman GA, Sun GY. Pro-inflammatory cytokines and lipopolysaccharide induce changes in cell morphology, and upregulation of ERK1/2, iNOS and sPLA(2)-IIA expression in astrocytes and microglia. J Neuroinflammation 2011, 8:121. 10.1186/1742-2094-8-121, 21943492.
47. Deshmukh VK, Raman PH, Dhuley JN, Naik SR. Role of ceruloplasmin in inflammation: increased serum ceruloplasmin levels during inflammatory conditions and its possible relationship with anti-inflammatory agents. Pharmacol Res Commun 1985, 17:633-642. 10.1016/0031-6989(85)90070-0, 4048245.
48. Engler R. Acute-phase proteins in inflammation. C R Seances Soc Biol Fil 1995, 189:563-578. 8564570.
49. Kang JH, Kim KS, Choi SY, Kwon HY, Won MH. Oxidative modification of human ceruloplasmin by peroxyl radicals. Biochim Biophys Acta 2001, 1568:30-36. 10.1016/S0304-4165(01)00198-2, 11731082.
50. Filipov NM, Seegal RF, Lawrence DA. Manganese potentiates in vitro production of proinflammatory cytokines and nitric oxide by microglia through a nuclear factor kappa B-dependent mechanism. Toxicol Sci 2005, 84:139-148. 10.1093/toxsci/kfi055, 15601679.
51. Zhang P, Lokuta KM, Turner DE, Liu B. Synergistic dopaminergic neurotoxicity of manganese and lipopolysaccharide: differential involvement of microglia and astroglia. J Neurochem 2010, 112:434-443. 10.1111/j.1471-4159.2009.06477.x, 19895668.
52. Kauppinen TM, Higashi Y, Suh SW, Escartin C, Nagasawa K, Swanson RA. Zinc triggers microglial activation. J Neurosci 2008, 28:5827-5835. 10.1523/JNEUROSCI.1236-08.2008, 18509044.
53. Mou YH, Yang JY, Cui N, Wang JM, Hou Y, Song S, Wu CF. Effects of cobalt chloride on nitric oxide and cytokines/chemokines production in microglia. Int Immunopharmacol 2012, 13:120-125. 10.1016/j.intimp.2012.03.017, 22472292.
54. Zhang Y, Brovkovych V, Brovkovych S, Tan F, Lee BS, Sharma T, Skidgel RA. Dynamic receptor-dependent activation of inducible nitric-oxide synthase by ERK-mediated phosphorylation of Ser745. J Biol Chem 2007, 282:32453-32461. 10.1074/jbc.M706242200, 17804409.
55. Huang SH, Jong AY. Cellular mechanisms of microbial proteins contributing to invasion of the blood-brain barrier. Cell Microbiol 2001, 3:277-287. 10.1046/j.1462-5822.2001.00116.x, 11298651.
56. Kim KS. Mechanisms of microbial traversal of the blood-brain barrier. Nat Rev Microbiol 2008, 6:625-634. 10.1038/nrmicro1952, 18604221.
57. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007, 87:315-424. 10.1152/physrev.00029.2006, 17237348.
58. Szabo C. Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 2003, 140-141:105-112. 10.1016/S0378-4274(02)00507-6, 12676456.
59. Loeffler DA, DeMaggio AJ, Juneau PL, Brickman CM, Mashour GA, Finkelman JH, Pomara N, LeWitt PA. Ceruloplasmin is increased in cerebrospinal fluid in Alzheimer's disease but not Parkinson's disease. Alzheimer Dis Assoc Disord 1994, 8:190-197. 10.1097/00002093-199408030-00005, 7986488.
60. Kuhlow CJ, Krady JK, Basu A, Levison SW. Astrocytic ceruloplasmin expression, which is induced by IL-1beta and by traumatic brain injury, increases in the absence of the IL-1 type 1 receptor. Glia 2003, 44:76-84. 10.1002/glia.10273, 12951659.
61. Loeffler DA, LeWitt PA, Juneau PL, Sima AA, Nguyen HU, DeMaggio AJ, Brickman CM, Brewer GJ, Dick RD, Troyer MD, Kanaley L. Increased regional brain concentrations of ceruloplasmin in neurodegenerative disorders. Brain Res 1996, 738:265-274. 10.1016/S0006-8993(96)00782-2, 8955522.
62. Hwang IK, Yoon DK, Yoo KY, Eum WS, Bahn JH, Kim DW, Kang JH, Kwon HY, Kang TC, Choi SY, Won MH. Ischemia-related change of ceruloplasmin immunoreactivity in neurons and astrocytes in the gerbil hippocampus and dentate gyrus. Neurochem Int 2004, 44:601-607. 10.1016/j.neuint.2003.10.002, 15016475.
63. Marques L, Auriac A, Willemetz A, Banha J, Silva B, Canonne-Hergaux F, Costa L. Immune cells and hepatocytes express glycosylphosphatidylinositol-anchored ceruloplasmin at their cell surface. Blood Cells Mol Dis 2012, 48:110-120. 10.1016/j.bcmd.2011.11.005, 22178061.
64. Banha J, Marques L, Oliveira R, Martins Mde F, Paixao E, Pereira D, Malho R, Penque D, Costa L. Ceruloplasmin expression by human peripheral blood lymphocytes: a new link between immunity and iron metabolism. Free Radic Biol Med 2008, 44:483-492. 10.1016/j.freeradbiomed.2007.10.032, 17991445.
65. Mazumder B, Mukhopadhyay CK, Prok A, Cathcart MK, Fox PL. Induction of ceruloplasmin synthesis by IFN-gamma in human monocytic cells. J Immunol 1997, 159:1938-1944. 9257859.
66. Skjorringe T, Moller LB, Moos T. Impairment of interrelated iron- and copper homeostatic mechanisms in brain contributes to the pathogenesis of neurodegenerative disorders. Front Pharmacol 2012, 3:169. 10.3389/fphar.2012.00169, 23055972.
67. Zheng W, Monnot AD. Regulation of brain iron and copper homeostasis by brain barrier systems: implication in neurodegenerative diseases. Pharmacol Ther 2012, 133:177-188. 10.1016/j.pharmthera.2011.10.006, 22115751.