Vinpocetine inhibits amyloid-beta induced activation of NF-κB, NLRP3 inflammasome and cytokine production in retinal pigment epithelial cells

Experimental Eye Research

Volumn 127, Issue , 2014, Pages 49-58

  Liu, Ruozhou Tom ^a   Wang, Aikun ^a   To, Eleanor ^a   Gao, Jiangyuan ^a   Cao, Sijia ^a   Cui, Jing Z ^a   Matsubara, Joanne A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

AMD; Amyloid ; Cytokine; Inflammasome; NF B; RPE; Vinpocetine

Indexed keywords

AMYLOID BETA PROTEIN; CRYOPYRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; TUMOR NECROSIS FACTOR ALPHA; VINPOCETINE; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; AMYLOID BETA PROTEIN[1-40]; CYTOKINE; INFLAMMASOME;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; FEMALE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; VITREOUS BODY; ANIMAL TISSUE; ANTIBODY LABELING; CYTOPLASM; DIET SUPPLEMENTATION; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; LYMPHOCYTE; MICROGLIA; RETINA PIGMENT CELL; WESTERN BLOTTING;

AMD; AMYLOID-Β; CYTOKINE; INFLAMMASOME; NF-ΚB; RPE; VINPOCETINE;

AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CELL LINE; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; INFLAMMASOMES; INJECTIONS, INTRAPERITONEAL; NF-KAPPA B; RATS; RATS, LONG-EVANS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RETINAL PIGMENT EPITHELIUM; VASODILATOR AGENTS; VINCA ALKALOIDS; VITREOUS BODY;

EID: 84904917944     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.07.003     Document Type: Article

References (51)

1. Anderson D.H., Mullins R.F., Hageman G.S., Johnson L.V. Arole for local inflammation in the formation of drusen in the aging eye. Am. J. Ophthalmol. 2002, 134:411-431.
2. Anderson D.H., Talaga K.C., Rivest A.J., Barron E., Hageman G.S., Johnson L.V. Characterization of β amyloid assemblies in drusen: the deposits associated with aging and age-related macular degeneration. Exp. Eye Res. 2004, 78:243-256.
3. Bauernfeind F.G., Horvath G., Stutz A., Alnemri E.S., MacDonald K., Speert D., Fernandes-Alnemri T., Wu J., Monks B.G., Fitzgerald K.A., Hornung V., Latz E. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J.Immunol. 2009, 183:787-791.
4. Bian Z.M., Elner S.G., Yoshida A., Elner V.M. Human RPE-monocyte co-culture induces chemokine gene expression through activation of MAPK and NIK cascade. Exp. Eye Res. 2003, 76:573-583.
5. Blackwell T.S., Christman J.W. The role of nuclear factor-kappa B in cytokine gene regulation. Am. J. Respir. Cell. Mol. Biol. 1997, 17:3-9.
6. Bouwmeester T., Bauch A., Ruffner H., Angrand P., Bergamini G., Croughton K., Cruciat C., Eberhard D., Gagneur J., Ghidelli S., Hopf C., Huhse B., Mangano R., Michon A., Schirle M., Schlegl J., Schwab M., Stein M.A., Bauer A., Casari G., Drewes G., Gavin A., Jackson D.B., Joberty G., Neubauer G., Rick J., Kuster B., Superti-Furga G. Aphysical and functional map of the human TNF-α/NF-κB signal transduction pathway. Nat. Cell. Biol. 2004, 6:97-105.
7. Chang S.H., Dong C. Signaling of interleukin-17 family cytokines in immunity and inflammation. Cell. Signal 2011, 23:1069-1075.
8. Chen Y., Kijlstra A., Chen Y., Yang P. IL-17A stimulates the production of inflammatory mediators via Erk1/2, p38 MAPK, PI3K/Akt, and NF-B pathways in ARPE-19 cells. Mol. Vis. 2011, 17:3072-3077.
9. Chen Y., Yang P., Li F., Kijlstra A. The effects of Th17 cytokines on the inflammatory mediator production and barrier function of ARPE-19 cells. PLoS One 2011, 6:e18139.
10. Di Virgilio F. The therapeutic potential of modifying inflammasomes and NOD-like receptors. Pharmacol. Rev. 2013, 65:872-905.
11. Dinarello C.A. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 2009, 27:519-550.
12. Ding J., Johnson L.V., Herrmann R., Farsiu S., Smith S.G., Groelle M., Mace B.E., Sullivan P., Jamison J.A., Kelly U., Harrabi O., Bollini S.S., Dilley J., Kobayashi D., Kuang B., Li W., Pons J., Lin J.C., Rickman C.B. Anti-amyloid therapy protects against retinal pigmented epithelium damage and vision loss in a model of age-related macular degeneration. Proc. Natl. Acad. Sci. USA 2011, 108:E279-E287.
13. Hageman G.S., Luthert P.J., Victor Chong N.H., Johnson L.V., Anderson D.H., Mullins R.F. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog. Retin. Eye Res. 2001, 20:705-732.
14. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-[beta]. Nat. Immunol. 2008, 9:857-865.
15. Isas J.M., Luibl V., Johnson L.V., Kayed R., Wetzel R., Glabe C.G., Langen R., Chen J. Soluble and mature amyloid fibrils in drusen deposits. Invest. Ophthalmol. Vis. Sci. 2010, 51:1304-1310.
16. Jeon K.I., Xu X., Aizawa T., Lim J.H., Jono H., Kwon D.S., Abe J., Berk B.C., Li J.D., Yan C. Vinpocetine inhibits NF-kappaB-dependent inflammation via an IKK-dependent but PDE-independent mechanism. Proc. Natl. Acad. Sci. USA 2010, 107:9795-9800.
17. Jiang K., To E., Cui J., Cao S., Gao J., Matsubara J. Drusen and pro-inflammatory mediators in the post-mortem human eye. J.Clin. Exp. Ophthalmol. 2012, 3:208. 10.4172/2155-9570.1000208.
18. Johnson L.V., Leitner W.P., Rivest A.J., Staples M.K., Radeke M.J., Anderson D.H. The Alzheimer's A beta -peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc. Natl. Acad. Sci. USA 2002, 99:11830-11835.
19. Kauppinen A., Niskanen H., Suuronen T., Kinnunen K., Salminen A., Kaarniranta K. Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells - implications for age-related macular degeneration (AMD). Immunol. Lett. 2012, 147:29-33.
20. Kavita U., Mizel S.B. Differential sensitivity of interleukin-1 alpha and -beta precursor proteins to cleavage by calpain, a calcium-dependent protease. J.Biol. Chem. 1995, 270:27758-27765.
21. Kerur N., Hirano Y., Tarallo V., Fowler B.J., Bastos-Carvalho A., Yasuma T., Yasuma R., Kim Y., Hinton D.R., Kirschning C.J., Gelfand B.D., Ambati J. TLR-independent and P2X7-dependent signaling mediate Alu RNA-induced NLRP3 inflammasome activation in geographic atrophy. Invest. Ophthalmol. Vis. Sci. 2013, 54:7395-7401.
22. Kim S.J., Ahn J.W., Kim H., Ha H.J., Lee S.W., Kim H.K., Lee S., Hong H.S., Kim Y.H., Choi C.Y. Two beta-strands of RAGE participate in the recognition and transport of amyloid-beta peptide across the blood brain barrier. Biochem. Biophys. Res. Commun. 2013, 439:252-257.
23. Kurji K.H., Cui J.Z., Lin T., Harriman D., Prasad S.S., Kojic L., Matsubara J.A. Microarray analysis identifies changes in inflammatory gene expression in response to amyloid-β stimulation of cultured human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 2010, 51:1151-1163.
24. Lee J., Rhee M.H., Kim E., Cho J.Y. BAY 11-7082 is a broad-spectrum inhibitor with anti-inflammatory activity against multiple targets. Mediat. Inflamm. 2012, 2012:416036.
25. Lemon B., Tjian R. Orchestrated response: a symphony of transcription factors for gene control. Genes. Dev. 2000, 14:2551-2569.
26. Lin T., Walker G.B., Kurji K., Fang E., Law G., Prasad S.S., Kojic L., Cao S., White V., Cui J.Z., Matsubara J.A. Parainflammation associated with advanced glycation endproduct stimulation of RPE invitro: implications for age-related degenerative diseases of the eye. Cytokine 2013, 62:369-381.
27. Liu R.T., Gao J., Cao S., Sandhu N., Cui J.Z., Chou C.L., Fang E., Matsubara J.A. Inflammatory mediators induced by amyloid-beta in the retina and RPE invivo: implications for inflammasome activation in age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2013, 54:2225-2237.
28. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell. 2002, 10:417-426.
29. Masters S.L., O'Neill L.A.J. Disease-associated amyloid and misfolded protein aggregates activate the inflammasome. Trends Mol. Med. 2011, 17:276-282.
30. Medina A.E. Vinpocetine as a potent antiinflammatory agent. Proc. Natl. Acad. Sci. USA 2010, 107:9921-9922.
31. Meneghini V., Bortolotto V., Francese M.T., Dellarole A., Carraro L., Terzieva S., Grilli M. High-mobility group box-1 protein and beta-amyloid oligomers promote neuronal differentiation of adult hippocampal neural progenitors via receptor for advanced glycation end products/nuclear factor-B axis: relevance for Alzheimer's disease. J.Neurosci. 2013, 33:6047-6059.
32. Mullins R.F., Russell S.R., Anderson D.H., Hageman G.S. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J. 2000, 14:835-846.
33. Nakazawa T., Kayama M., Ryu M., Kunikata H., Watanabe R., Yasuda M., Kinugawa J., Vavvas D., Miller J.W. Tumor necrosis factor-alpha mediates photoreceptor death in a rodent model of retinal detachment. Invest. Ophthalmol. Vis. Sci. 2011, 52:1384-1391.
34. Napetschnig J., Wu H. Molecular basis of NF-κB signaling. Annu. Rev. Biophys. 2013, 42:443-468.
35. Ning A., Cui J., To E., Ashe K.H., Matsubara J. Amyloid-β deposits lead to retinal degeneration in a mouse model of Alzheimer Disease. Invest. Ophthalmol. Vis. Sci. 2008, 49:5136-5143.
36. Nivison-Smith L., Acosta M.L., Misra S., O'Brien B.J., Kalloniatis M. Vinpocetine regulates cation channel permeability of inner retinal neurons in the ischaemic retina. Neurochem. Int. 2014, 66C:1-14.
37. Pereira C., Agostinho P., Oliveira C.R. Vinpocetine attenuates the metabolic dysfunction induced by amyloid beta-peptides in PC12 cells. Free Radic. Res. 2000, 33:497-506.
38. Polgar M., Vereczkey L., Nyary I. Pharmacokinetics of vinpocetine and its metabolite, apovincaminic acid, in plasma and cerebrospinal fluid after intravenous infusion. J.Pharm. Biomed. Anal. 1985, 3:131-139.
39. Prakasam A., Muthuswamy A., Ablonczy Z., Greig N.H., Fauq A., Rao K.J., Pappolla M.A., Sambamurti K. Differential accumulation of secreted AbetaPP metabolites in ocular fluids. J.Alzheimer's Dis. 2010, 20:1243-1253.
40. Seddon J.M., George S., Rosner B., Rifai N. Progression of age-related macular degeneration: prospective assessment of C-reactive protein, interleukin 6, and other cardiovascular biomarkers. Arch. Ophthalmol. 2005, 123:774-782.
41. Segovia J., Sabbah A., Mgbemena V., Tsai S.Y., Chang T.H., Berton M.T., Morris I.R., Allen I.C., Ting J.P., Bose S. TLR2/MyD88/NF-kB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 2012, 7:e29695.
42. Strowig T., Henao-Mejia J., Elinav E., Flavell R. Inflammasomes in health and disease. Nature 2012, 481:278-286.
43. Szatmari S.Z., Whitehouse P.J. Vinpocetine for cognitive impairment and dementia. Cochrane Database Syst. Rev. 2003, 1:CD003119.
44. Tamaki N., Matsumoto S. Agents to improve cerebrovascular circulation and cerebral metabolism - vinpocetine. Nihon Rinsho 1985, 43:376-378.
45. Tarallo V., Hirano Y., Gelfand B., Dridi S., Kerur N., Kim Y., Cho W., Kaneko H., Fowler B., Bogdanovich S., Albuquerque R.C., Hauswirth W., Chiodo V., Kugel J., Goodrich J., Ponicsan S., Chaudhuri G., Murphy M., Dunaief J., Ambati B., Ogura Y., Yoo J., Lee D., Provost P., Hinton D., Núñez G., Baffi J., Kleinman M., Ambati J. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 2012, 149:847-859.
46. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 2004, 122:564-572. The Eye Diseases Prevalence Research Group.
47. Tschopp J., Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production?. Nat. Rev. Immunol. 2010, 10:210-215.
48. Tseng W.A., Thein T., Kinnunen K., Lashkari K., Gregory M.S., D'Amore P.A., Ksander B.R. NLRP3 inflammasome activation in retinal pigment epithelial cells by lysosomal destabilization: implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2013, 54:110-120.
49. Xu H., Chen M., Forrester J.V. Para-inflammation in the aging retina. Prog. Retin. Eye Res. 2009, 28:348-368.
50. Yazdi A.S., Guarda G., Riteau N., Drexler S.K., Tardivel A., Couillin I., Tschopp J. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc. Natl. Acad. Sci. USA 2010, 107:19449-19454.
51. Zhao Y.Y., Yu J.Z., Li Q.Y., Ma C.G., Lu C.Z., Xiao B.G. TSPO-specific ligand Vinpocetine exerts a neuroprotective effect by suppressing microglial inflammation. Neuron. Glia Biol. 2011, 7:187-197.