Neuropeptide y inhibits interleukin-1 beta-induced microglia motility

Journal of Neurochemistry

Volumn 120, Issue 1, 2012, Pages 93-105

  Ferreira, Raquel ^a   Santos, Tiago ^a   Cortes, Luísa ^a   Cochaud, Stéphanie ^a   Agasse, Fabienne ^a   Silva, Ana Paula ^b   Xapelli, Sara ^a   Malva, João O ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

inflammation; lipopolysaccharide; microglia; migration; p38

Indexed keywords

CD11B ANTIGEN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROPEPTIDE Y; NEUROPEPTIDE Y1 RECEPTOR;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL MEMBRANE; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MICROGLIA; MOUSE; NERVE CELL STIMULATION; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM;

ANIMALS; ANTIGENS, CD11B; BLOTTING, WESTERN; CELL LINE; CELL MOVEMENT; CEREBRAL CORTEX; CYTOSKELETON; DATA INTERPRETATION, STATISTICAL; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICROGLIA; NEUROPEPTIDE Y; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, NEUROPEPTIDE Y;

EID: 83855162714     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07541.x     Document Type: Article

References (67)

1. Abreu M. T., and, Arditi M., (2004) Innate immunity and toll-like receptors: clinical implications of basic science research. J. Pediatr. 144, 421-429. (Pubitemid 38457342)
2. Agasse F., Bernardino L., Kristiansen H., Christiansen S. H., Ferreira R., Silva B., Grade S., Woldbye D. P. D., and, Malva J. O., (2008) Neuropeptide Y promotes neurogenesis in murine subventricular zone. Stem Cells 26, 1636-1645.
3. Ahmed A. A., Wahbi A., Nordlind K., Kharazmi A., Sundqvist K. G., Mutt M., and, Lidén S., (1998) In vitro leishmania major promastigote-induced macrophage migration is modulated by sensory and autonomic neuropeptides. Scand. J. Immunol., 48, 79-85. (Pubitemid 28329156)
4. Allan S. M., (2005) Pragmatic target discovery from novel gene to functionally defined drug target. Methods Mol. Med. 104, 333-346.
5. Allan S. M., and, Rothwell N. J., (2003) Inflammation in central nervous system injury. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 1669-1677. (Pubitemid 37298635)
6. Arend W. P., Welgus H. G., Thompson R. C., and, Eisenberg S. P., (1990) Biological properties of recombinant human monocyte-derived interleukin 1 receptor antagonist. J. Clin. Invest. 85, 1694-1697. (Pubitemid 20176469)
7. Bedoui S., Kawamura N., Straub R. H., Pabst R., Yamamura T., and, von Hörsten S., (2003a) Relevance of Neuropeptide Y for the neuroimmune crosstalk. J. Neuroimmunol. 134, 1-11. (Pubitemid 36050825)
8. Bedoui S., Miyake S., Lin Y., Miyamoto K., Oki S., Kawamura N., Beck-Sickinger A., von Horsten S., and, Yamamura T., (2003b) Neuropeptide Y (NPY) Suppresses Experimental Autoimmune Encephalomyelitis: NPY1 Receptor-Specific Inhibition of Autoreactive Th1 Responses In Vivo. J. Immunol. 171, 3451-3458. (Pubitemid 37254546)
9. Bedoui S., von Hörsten S., and, Gebhardt T., (2007) A role for neuropeptide Y (NPY) in phagocytosis: Implications for innate and adaptive immunity. Peptides 28, 373-376. (Pubitemid 46176264)
10. Ben-Levy R., Leighton I. A., Doza Y. N., Attwood P., Morrice N., Marshall C. J., and, Cohen P., (1995) Identification of novel phosphorylation sites required for activation of MAPKAP kinase-2. EMBO J. 14, 5920-5930.
11. Bernardino L., Ferreira R., Cristõvão A. J., Sales F., and, Malva J. O., (2005a) Inflammation and neurogenesis in temporal lobe epilepsy. Curr. Drug Targets CNS Neurol. Disord. 4, 349-360. (Pubitemid 41086755)
12. Bernardino L., Xapelli S., Silva A. P., Jakobsen B., Poulsen F. R., Oliveira C. R., Vezzani A., Malva J. O., and, Zimmer J., (2005b) Modulator effects of interleukin-1β and tumor necrosis factor-α on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 25, 6734-6744. (Pubitemid 41023141)
13. Bernardino L., Balosso S., Ravizza T., Marchi N., Ku G., Randle J. C., Malva J. O., and, Vezzani A., (2008) Inflammatory events in hippocampal slice cultures prime neuronal susceptibility to excitotoxic injury: a crucial role of P2X7 receptor-mediated IL-1β release. J. Neurochem. 106, 271-280. (Pubitemid 351840213)
14. Block M. L., Zecca L., and, Hong J.-S., (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurol. 8, 57-69. (Pubitemid 46011999)
15. Brakch N., Allemandou F., Cavadas C., Grouzmann E., and, Brunner H. R., (2002) Dibasic cleavage site is required for sorting to the regulated secretory pathway for both pro- and neuropeptide Y. J. Neurochem. 81, 1166-1175. (Pubitemid 34809251)
16. Cartier L., Hartley O., Dubois-Dauphin M., and, Krause K.-H., (2005) Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res. Rev. 48, 16-42. (Pubitemid 40215781)
17. Chen L. Y., and, Pan Z. K., (2009) Synergistic activation of leukocytes by bacterial chemoattractants: potential drug targets. Endocr. Metab. Immune Disord. Drug Targets 9, 361-370.
18. Choi J., and, Koh S., (2008) Role of brain inflammation in epileptogenesis. Yonsei Med. J. 49, 1-18. (Pubitemid 351513640)
19. Cohen J., (2002) The immunopathogenesis of sepsis. Nature 420, 885-891. (Pubitemid 36019643)
20. Danton G. H., and, Dietrich W. D., (2003) Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 62, 127-136. (Pubitemid 36176947)
21. De la Fuente M., Bernaez I., Del Rio M., and, Hernanz A., (1993) Stimulation of murine peritoneal macrophage functions by neuropeptide Y and peptide YY. Involvement of protein kinase C. Immunology 80, 259-265. (Pubitemid 23308581)
22. Deng C., Radu C., Diab A., Tsen M. F., Hussain R., Cowdery J. S., Racke M. K., and, Thomas J. A., (2003) IL-1 receptor-associated kinase 1 regulates susceptibility to organ-specific autoimmunity. J. Immunol. 170, 2833-2842. (Pubitemid 36302153)
23. Dinarello C. A., (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550.
24. El Bahh B., Balosso S., Hamilton T., Herzog H., Beck-Sickinger A. G., Sperk G., Gehlert D. R., Vezzani A., and, Colmers W. F., (2005) The anti-epileptic actions of neuropeptide Y in the hippocampus are mediated by Y2 and not Y5 receptors. Eur. J. Neurosci. 22, 1417-1430. (Pubitemid 41442414)
25. Fantuzzi G., and, Dinarello C. A., (1999) Interleukin-18 and interleukin-1β: two cytokine substrates for ICE (caspase-1). J. Clin. Immunol. 19, 1-11. (Pubitemid 29113328)
26. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Melchiorri L., Baricordi O., and, Di Virgilio F., (1997) Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 159, 1451-1458. (Pubitemid 127484125)
27. Ferreira R., Xapelli S., Santos T., Silva A. P., Cristovao A., Cortes L., and, Malva J. O., (2010) Neuropeptide Y modulation of interleukin-1β (IL-1β)-induced nitric oxide production in microglia. J. Biol. Chem. 285, 41921-41934.
28. Furundzija V., Fritzsche J., Kaufmann J., Meyborg H., Fleck E., Kappert K., and, Stawowy P., (2010) IGF-1 increases macrophage motility via PKC/p38-dependent αvβv3-integrin inside-out signaling. Biochem. Biophys. Res. Commun. 394, 786-791.
29. Gan L., and, Li L., (2010) Interleukin-1 receptor-associated kinase-1 (IRAK-1) functionally associates with PKC[var epsilon] and VASP in the regulation of macrophage migration. Mol. Immunol. 47, 1278-1282.
30. Garden G., and, Möller T., (2006) Microglia biology in health and disease. J. Neuroimmune Pharmacol. 1, 127-137. (Pubitemid 44257488)
31. Grahames C. B. A., Michel A. D., Chessell I. P., and, Humphrey P. P. A., (1999) Pharmacological characterization of ATP- and LPS-induced IL-1B release in human monocytes. Br. J. Pharmacol. 127, 1915-1921. (Pubitemid 29392888)
32. Griffiths R., Stam E., Downs J., and, Otterness I., (1995) ATP induces the release of IL-1 from LPS-primed cells in vivo. J. Immunol. 154, 2821-2828.
33. von Holst H., Rudehill A., and, Lundberg J. M., (1991) Neuropeptide Y levels in central and peripheral cerebrospinal fluid in patients with intracranial disorders. Acta Neurochir. (Wien) 112, 132-135.
34. Huang C., Jacobson K., and, Schaller M. D., (2004) MAP kinases and cell migration. J. Cell Sci. 117, 4619-4628. (Pubitemid 39433429)
35. Kawai T., and, Akira S., (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384.
36. Kettenmann H., Hanisch U. K., Noda M., and, Verkhratsky A., (2011) Physiology of microglia. Physiol. Rev. 91, 461-553.
37. Koistinaho M., and, Koistinaho J., (2002) Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40, 175-183. (Pubitemid 35337375)
38. Koning N., Uitdehaag B. M. J., Huitinga I., and, Hoek R. M., (2009) Restoring immune suppression in the multiple sclerosis brain. Prog. Neurobiol. 89, 359-368.
39. Kyrkanides S., Olschowka J. A., Williams J. P., Hansen J. T., and, O'Banion M. K., (1999) TNF-α and IL-1β mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury. J. Neuroimmunol. 95, 95-106. (Pubitemid 29173026)
40. Minghetti L., Ajmone-Cat M. A., De Berardinis M. A., and, De Simone R., (2005) Microglial activation in chronic neurodegenerative diseases: roles of apoptotic neurons and chronic stimulation. Brain Res. Rev. 48, 251-256. (Pubitemid 40585756)
41. Nadler J. V., Tu B., Timofeeva O., Jiao Y., and, Herzog H., (2007) Neuropeptide Y in the recurrent mossy fiber pathway. Peptides 28, 357-364. (Pubitemid 46176247)
42. Nave H., Bedoui S., and, Moenter F., et al. (2004) Reduced tissue immigration of monocytes by neuropeptide Y during endotoxemia is associated with Y2 receptor activation. J. Neuroimmunol. 155, 1-12. (Pubitemid 39165772)
43. Nguyen J., Gogusev J., Knapnougel P., and, Bauvois B., (2006) Protein tyrosine kinase and p38 MAP kinase pathways are involved in stimulation of matrix metalloproteinase-9 by TNF-α in human monocytes. Immunol. Lett. 106, 34-41. (Pubitemid 44093049)
44. Nick J. A., Young S. K., Brown K. K., Avdi N. J., Arndt P. G., Suratt B. T., Janes M. S., Henson P. M., and, Worthen G. S., (2000) Role of p38 mitogen-activated protein kinase in a murine model of pulmonary inflammation. J. Immunol. 164, 2151-2159. (Pubitemid 30108774)
45. Nimmerjahn A., Kirchhoff F., and, Helmchen F., (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318. (Pubitemid 40746128)
46. Ogura M., and, Kitamura M., (1998) Oxidant stress incites spreading of macrophages via extracellular signal-regulated kinases and p38 mitogen-activated protein kinase. J. Immunol. 161, 3569-3574.
47. Perry V. H., Nicoll J. A. R., and, Holmes C., (2010) Microglia in neurodegenerative disease. Nat. Rev. Neurol. 6, 193-201.
48. Pinheiro P. S., Rodrigues R. J., Rebola N., Xapelli S., Oliveira C. R., and, Malva J. O., (2005) Presynaptic kainate receptors are localized close to release sites in rat hippocampal synapses. Neurochem. Int. 47, 309-316. (Pubitemid 40968015)
49. Pinteaux E., Trotter P., and, Simi A., (2009) Cell-specific and concentration-dependent actions of interleukin-1 in acute brain inflammation. Cytokine 45, 1-7.
50. Prod'homme T., Weber M. S., Steinman L., and, Zamvil S. S., (2006) A neuropeptide in immune-mediated inflammation, Y? Trends Immunol. 27, 164-167.
51. Ridley A. J., Schwartz M. A., Burridge K., Firtel R. A., Ginsberg M. H., Borisy G., Parsons J. T., and, Horwitz A. R., (2003) Cell migration: integrating signals from front to back. Science 302, 1704-1709. (Pubitemid 37505725)
52. Rivest S., (2003) Molecular insights on the cerebral innate immune system. Brain Behav. Immun. 17, 13-19. (Pubitemid 36207597)
53. Santos A. E., Carvalho A. L., Lopes M. C., and, Carvalho A. P., (2001) Differential postreceptor signaling events triggered by excitotoxic stimulation of different ionotropic glutamate receptors in retinal neurons. J. Neurosci. Res. 66, 643-655. (Pubitemid 33032333)
54. Shen A., Yang J., and, Gu Y., et al. (2008) Lipopolysaccharide-evoked activation of p38 and JNK leads to an increase in ICAM-1 expression in Schwann cells of sciatic nerves. FEBS J. 275, 4343-4353.
55. Shi Y., and, Gaestel M., (2002) In the cellular garden of forking paths: how p38 MAPKs signal for downstream assistance. Biol. Chem. 383, 1519-1536. (Pubitemid 35282972)
56. Silva A. P., Cavadas C., and, Grouzmann E., (2002) Neuropeptide Y and its receptors as potential therapeutic drug targets. Clin. Chim. Acta 326, 3-25. (Pubitemid 35341161)
57. Silva A. P., Pinheiro P. S., Carvalho A. P., Carvalho C. M., Jakobsen B., Zimmer J., and, Malva J. O., (2003) Activation of neuropeptide Y receptors is neuroprotective against excitotoxicity in organotypic hippocampal slice cultures. FASEB J. 21, 671-681.
58. Small J. V., Rottner K., and, Kaverina I., (1999) Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11, 54-60. (Pubitemid 29084132)
59. ÅsmiaÅowska M., Domin H., Zieba B., Koaniewska E., Michalik R., Piotrowski P., and, Kajta M., (2009) Neuroprotective effects of neuropeptide Y-Y2 and Y5 receptor agonists in vitro and in vivo. Neuropeptides 43, 235-249.
60. Turrin N., and, Rivest S., (2006) Molecular and cellular immune mediators of neuroprotection. Mol. Neurobiol. 34, 221-242.
61. Valster A., Tran N. L., Nakada M., Berens M. E., Chan A. Y., and, Symons M., (2005) Cell migration and invasion assays. Methods 37, 208-215. (Pubitemid 41587431)
62. Vetvicka V., Hanikyrova M., Vetvickova J., and, Ross G. D., (1999) Regulation of CR3 (CD11b/CD18)-dependent natural killer (NK) cell cytotoxicity by tumour target cell MHC class I molecules. Clin. Exp. Immunol. 115, 229-235. (Pubitemid 29052447)
63. Vezzani A., and, Granata T., (2005) Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46, 1724-1743. (Pubitemid 44921957)
64. Wang S. J., (2005) Activation of neuropeptide Y Y1 receptors inhibits glutamate release through reduction of voltage-dependent Ca2+ entry in the rat cerebral cortex nerve terminals: suppression of this inhibitory effect by the protein kinase C-dependent facilitatory pathway. Neuroscience 134, 987-1000.
65. Wheway J., Herzog H., and, Mackay F., (2007) NPY and receptors in immune and inflammatory diseases. Curr. Top. Med. Chem. 7, 1743-1752. (Pubitemid 350131011)
66. Woo C. H., Lim J. H., and, Kim J. H., (2004) Lipopolysaccharide induces matrix metalloproteinase-9 expression via a mitochondrial reactive oxygen species-p38 kinase-activator protein-1 pathway in raw 264.7 cells. J. Immunol. 173, 6973-6980.
67. Xapelli S., Bernardino L., and, Ferreira R., et al. (2008) Interaction between neuropeptide Y (NPY) and brain-derived neurotrophic factor in NPY-mediated neuroprotection against excitotoxicity: a role for microglia. Eur. J. Neurosci. 27, 2089-2102. (Pubitemid 351521490)