Vasoactive intestinal peptide protects against β-amyloid-induced neurodegeneration by inhibiting microglia activation at multiple levels

GLIA

Volumn 56, Issue 10, 2008, Pages 1091-1103

  Delgado, Mario ^a   Varela, Nieves ^a   Gonzalez Rey, Elena ^b  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Alzheimer's disease; Cytokines; Inflammation; Neuroimmunology; Neuropeptides; Signal transduction; Transcription factors

Indexed keywords

AMYLOID BETA PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DRUG EFFICACY; EMBRYO; IN VIVO STUDY; MICROGLIA; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN; ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; INFLAMMATION MEDIATORS; MICE; MICE, INBRED BALB C; MICROGLIA; NERVE DEGENERATION; NEURONS; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION; VASOACTIVE INTESTINAL PEPTIDE;

EID: 51349161367     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20681     Document Type: Article

References (63)

1. Arai H, Moroji T, Kosaka K. 1984. Somatostatin and vasoactive intestinal polypeptide in postmortem brains from patients with Alzheimer-type dementia. Neurosci Lett 52:73-78.
2. Baldwin A. 1996. The NF-κB, I κB proteins: new discoveries and insights. Annu Rev Immunol 14:649-681.
3. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Ehan K, Eholodenko D, Lee M, Lieberbug I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T. 2000. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
4. Brenneman DE. 2007. Neuroprotection: a comparative view of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Peptides 28:1720-1726.
5. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK. 1992. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol 149:2736-2741.
6. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE. 2000. Inflammatory mechanisms in Alzheimer's disease: inhibition of β-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARγ agonists. J Neurosci 20:558-567.
7. D'Alimonte I, Flati V, D'Auro M, Toniato E, Martinotti S, Rathbone MP, Jiang S, Ballerini P, Di Iorio P, Caciagli F, Ciccarelli R. 2007. Guanosine inhibits CD40 receptor expression and function induced by cytokines and β amyloid in mouse microglia cells. J Immunol 178: 720-731.
8. Dawson TM, Dawson VL. 2002. Neuroprotective and neurorestorative strategies for Parkinson's disease. Nat Neurosci 5:1058-1061.
9. Dejda A, Sokolowska P, Nowak JZ. 2005. Neuroprotective potential of three neuropeptides PACAP, VIP and PHI. Pharmacol Rep 57:307-320.
10. Delgado M. 2002. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit CBP-NF-κB interaction in activated microglia. Biochem Biophys Res Commun 297:1181-1185.
11. Delgado M. 2003. Inhibition of interferon (IFN) γ-induced Jak-STAT1 activation in microglia by vasoactive intestinal peptide: inhibitory effect on CD40, IFN-induced protein-10, and inducible nitric-oxide synthase expression. J Biol Chem 278:27620-27629.
12. Delgado M, Ganes. D. 2001. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit nuclear factor-κB-dependent gene activation at multiple levels in the human monocytic cell line THP-1. J Biol Chem 276:369-380.
13. Delgado M, Ganea D. 2003a. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J 17:1922-1924.
14. Delgado M, Ganea D. 2003b. Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation. FASEB J 17:944-946.
15. Delgado M, Jonakait GM, Ganea D. 2002. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit chemokine production in activated microglia. Glia 39:148-161.
16. Delgado M, Leceta J, Ganea D. 2003. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia. J Leukoc Biol 73:155-164.
17. Delgado M, Pozo D, Ganes, D. 2004. The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol Rev 56:249-290.
18. Derijard B, Raingeaud J, Barrett T, Wu L-H, Ham L, Ulevitch RJ, Davis RJ. 1995. Independent human MAP-kinase signal transduction pathways defined by MEK, MKK isoforms. Science 267:682-685.
19. Dickson DW, Farlo J, Davies P, Crystal H, Fuld P, Yen SH. 1988. Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. Am J Pathol 132:86-101.
20. Dickson DW, Lee SC, Mattiace LA, Yen SC, Brosnan CF. 1993. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7:75-83.
21. Emson PC, Fahremkrug J, Spokes EG. 1979. Vasoactive intestinal peptide (VIP): distribution in normal human brain and in Hutington's disease. Brain Res 173:174-178.
22. Franciosi S, Ryu JK, Choi HB, Radov L, Kim SU, McLarnon JG. 2006. Broad-spectrum effects of 4-aminopyridine to modulate amyloid β1-42-induced cell signaling and functional responses in human microglia. J Neurosci 26:11652-11664.
23. Giovannini MG, Scali C, Prosperi C, Bellucci A, Vannucchi MG, Rosi S, Pepeu G, Casamenti F. 2002. β-Amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: involvement of the p38MAPK pathway. Neurobiol Dis 11:257-274.
24. Glowa JR, Panlilio LV, Brenneman DE, Gozes I, Fridkin M, Hill JM. 1992. Learning impairment following intracerebral administration of the HIV envelope protein gp120 or a VIP antagonist. Brain Res 570:49-53.
25. Gonzalez-Rey E, Chorny A, Delgado M. 2007. Regulation of immune tolerance by anti-inflammatory neuropeptides. Nat Rev Immunol 7:52-63.
26. Gonzalez-Rey E, Delgado M. 2007. Anti-inflammatory neuropeptide receptors: new therapeutic targets for immune disorders? Trends Pharmacol Sci 28:482-491.
27. Gonzalez-Scarano F, Baltuch G. 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219-240.
28. Gourlet P, De Neef P, Cnudde J, Waelbroeck M, Robberecht P. 1997. In vitro properties of a high affinity selective antagonist of the VIP1 receptor. Peptides 18:1555-1560.
29. Gourlet P, Vandermeers A, Vertongen P, Ratche J, De Neef P, Cnudde J, Waelbroeck M, Robberecht P. 1996. Development of high affinity selective VIP1 receptor agonists. Peptides 18:1539-1545.
30. Gozes I, Bardea A, Reshef A, Zamostiano R, Zhukovsky S, Rubinraut S, Fridkin M, Brenneman DE. 1996. Neuroprotective strategy for Alzheimer disease: intranasal administration of a fatty neuropeptide. Proc Natl Acad Sci USA 93:427-432.
31. Gozes I, Glowa J, Brenneman DE, McCune SK, Lee E, Westphal H. 1993. Learning and sexual deficiencies in transgenic mice carrying a chimeric vasoactive intestinal peptide gene. J Mol Neurosci 4:185-193.
32. Gozes I, Schachter P, Shani Y, Giladi E. 1988. Vasoactive intestinal peptide gene expression from embryos to aging rats. Neuroendocrinology 47:27-31.
33. Harmar AJ, Arimura A, Gozes I, Journot L, Laburthe M, Pisegna JR, Rawlings SR, Robberecht P, Said SI, Sreedharan SP, Wank SA, Washeck JA. 1998. International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol Rev 50:625-627.
34. Hokari R, Lee H, Crawley SC, Yang SC, Gum JR Jr, Miura S, Kim YS. 2005. Vasoactive intestinal peptide upregulates MUC2 intestinal mucin via CREB/ ATF1. Am J Physiol Gastrointest Liver Physiol 289:G949-G959.
35. Kalaria RN. 1999. Microglia and Alzheimer's disease. Curr Opin Hematol 6:15-24.
36. Kim W, Mohney RP, Wilson B, Jeohn G, Liu B, Hong J. 2000. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20:6309-6316.
37. Koh JY, Choi DW. 1987. Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Meth 20:83-90.
38. Koistinaho M, Koistinaho J. 2002. Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40:175-183.
39. Kwok RPS, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SGE, Green MR, Goodman RH. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223-226.
40. Mackenzie IR, Munoz DG. 1998. Nonsteroidal anti-inflammatory drug use and Alzheimer-type pathology in aging. Neurology 50:986-990.
41. McDonald DR, Bamberger M, Combs C, Landreth GE. 1998. β-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J Neurosci 18:4451-4460.
42. McDonald DR, Brunden KR, Landreth GE. 1997. Amyloid fibrils activate tyrosine kinase-dependent signaling and superoxide production in microglia. J Neurosci 17:2284-2294.
43. McGeer EG, McGeer PL. 1998. The importance of inflammatory mechanisms in Alzheimer disease. Exp Gerontol 33:371-378.
44. McGeer PL, Itagaki S, Tago H, McGeer EG. 1987. Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci Lett 79:195-200.
45. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG. 1993. Microglia in degenerative neurological disease. Glia 7:84-92.
46. McGeer PL, McGeer EG. 1999. Inflammation of the brain in Alzheimer's disease: implications for therapy. J Leukoc Biol 65:409-415.
47. McGeer PL, Rogers J. 1992. Anti-inflammatory agents as a therapeutic approach to Alzheimer's disease. Neurology 42:447-449.
48. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, Ferrari D, Rossi F. 1995. Activation of microglial cells by β-amyloid protein and interferon-. Nature 374:647-650.
49. Miller G. 2005. Neuroscience. The dark side of glia. Science 308:778-781.
50. Moro O, Lerner EA. 1996. Maxadilan, the vasodilator from sand flies, is a specific pituitary adenylate cyclase activating peptide type I receptor agonist. J Biol Chem 271:966-970.
51. Onoue S, Endo K Ohshima K, Yajima T, Kashimoto K. 2002. The neuropeptide PACAP attenuates β-amyloid (1-42)-induced toxicity in PC12 cells. Peptides 23:1471-1478.
52. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R. 2002. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278:13309-13317.
53. Ranaivo HR, Craft JM, Hu W, Guo L, Wing LK,Van Eldik LJ, Watterson DM. 2006. Glia as a therapeutic target: selective suppression of human amyloid-p-induced upregulation of brain proinflammatory cytokine production attenuates neurodegeneration. J Neurosci 26: 662-670.
54. Rich JB, Rasmusson DX, Folstein MF, Carson KA, Kawas C, Brandt J. 1995. Nonsteroidal anti-inflammatory drugs in Alzheimer's disease. Neurology 45:51-55.
55. Rogers J, Kirby LC, Hempelman SR, Berry DL, McGeer PL, Kaszniak AW, Zalinski J, Cofield M, Mansukhani L, Willson P, Kogan F. 1993. Clinical trial of indomethacin in Alzheimer's disease. Neurology 43: 1609-1611.
56. Romano D, Magalon K, Ciampini A, Talet C, Enjalbert A, Gerard C. 2003. Differential involvement of the Ras and Rap1 small GTPases in vasoactive intestinal and pituitary adenylyl cyclase activating polypeptides control of the prolactin gene. J Biol Chem 278:51386-51394.
57. Stewart WF, Kawas C, Corrada M, Metter EJ. 1997. Risk of Alzheimer's disease and duration of NSAID use. Neurology 48:626-632.
58. Tuppo EE, Arias HR. 2005. The role of inflammation in Alzheimer's disease. Int J Biochem Cell Biol 37:289-305.
59. Weldon DT, Rogers SD, Ghilardi A, Finke MP, Cleary JP, O'Hare E, Esler WP, Maggio JE, Mantyh PW. 1998. Fibrillar β-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo. J Neurosci 18:2161-2173.
60. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde B, McConlogue L, Masliah E, Mucke L. 2001. TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice. Nat Med 7:612-618.
61. Xia M, Sreedharan SP, Bolin DR, Gaufo GO, GoetzI EJ. 1997. Novel cyclic peptide agonist of high potency and selectivity for the type II vasoactive intestinal peptide receptor. J Pharmacol Exp Ther 281:629-633.
62. Xie Z, Wei M, Morgan TE, Fabrizio P, Han D, Finch CE, Longo VD. 2002. Peroxynitrite mediates neurotoxicity of amyloid β-peptidel-42-and lipopolysaccharide-activated microglia. J Neurosci 22:3484-3492.
63. Zhou JN, Hofman MA, Swaab DF. 1995. VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease. Neurobiol Aging 16:571-576.