Bindarit, inhibitor of CCL2 synthesis, protects neurons against amyloid-β-induced toxicity

Journal of Alzheimer's Disease

Volumn 38, Issue 2, 2014, Pages 281-293

  Severini, Cinzia ^a   Passeri, Pamela Petrocchi ^b   Ciotti, Mariateresa ^b   Florenzano, Fulvio ^c   Possenti, Roberta ^b,d   Zona, Cristina ^b,d   Di Matteo, Anna ^e   Guglielmotti, Angelo ^e   Calissano, Pietro ^c   Pachter, Joel ^f   Mercanti, Delio ^b  

^a INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^b CNR   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e Università Politecnica delle Marche ACRAF Gruppo Angelini   (Italy)

^f UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Alzheimer's disease; amyloid toxicity; bindarit; CCL2; neuroinflammation

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN[25-35]; BINDARIT; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY; DOSE RESPONSE; EMBRYO; FEMALE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

ALZHEIMER'S DISEASE; AMYLOID-Β TOXICITY; BINDARIT; CCL2; NEUROINFLAMMATION;

ADENOSINE TRIPHOSPHATE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL SURVIVAL; CEREBRAL CORTEX; CHEMOKINE CCL2; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; INDAZOLES; NEUROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; PREGNANCY; PROPIONATES; RATS; RATS, WISTAR;

EID: 84889606928     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131070     Document Type: Article

References (59)

1. Selkoe DJ (2001) Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 8, 741-766. (Pubitemid 32267077)
2. Selkoe DJ (1994) Amyloid beta-protein precursor: New clues to the genesis of Alzheimer's disease. Curr Opin Neurobiol 4, 708-716.
3. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21, 383-421. (Pubitemid 30349107)
4. McGeer PL, McGeer EG (2002) Local neuroinflammation and the progression of Alzheimer's disease. J Neurovirol 8, 529-538. (Pubitemid 36104718)
5. Mrak RE, Griffin WS (2005) Glia and their cytokines in progression of neurodegeneration. Neurobiol Aging 26, 349-354. (Pubitemid 40082718)
6. Luster AD (1998) Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 338, 436-445. (Pubitemid 28135672)
7. Hesselgesser J, Horuk R (1999) Chemokine and chemokine receptor expression in the central nervous system. J Neurovirol 5, 13-26. (Pubitemid 29051874)
8. Asensio VC, Campbell IL (1999) Chemokines in the CNS: Plurifunctional mediators in diverse states. Trends Neurosci 22, 504-512. (Pubitemid 29481851)
9. Rubio-Perez JM,Morillas-Ruiz JM (2012) A review: Inflammatory process in Alzheimer's disease, role of cytokines. ScientificWorldJournal 2012, 756357.
10. Xia M, Hyman BT (1999) Chemokines/chemokine receptors in the central nervous system and Alzheimer's disease. J Neurovirol 5, 32-41. (Pubitemid 29051876)
11. Mines M, Ding Y, Fan GH (2007) The many roles of chemokine receptors in neurodegenerative disorders: Emerging new therapeutical strategies. Curr Med Chem 14, 2456-2470. (Pubitemid 47618034)
12. Galimberti D, Scarpini E, Scheltens P (2003) On behalf of the DIAR Group. Chemokines in serum and CSF of Alzheimer's disease patients. Ann Neurol 53, 547-548. (Pubitemid 36373272)
13. Galimberti D, Schoonenboom N, Scheltens P, Fenoglio C, Bouwman F,Venturelli E, Guidi I, Blankenstein MA, Bresolin N, Scarpini E (2006) Intrathecal chemokine synthesis in mild cognitive impairment and Alzheimer disease. Arch Neurol 63, 538-543.
14. Conductier G, Blondeau N, Guyon A, Nahon JL, Rov̀ere C (2010) The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J Neuroimmunol 224, 93-100.
15. Westin K, Buchhave P, Nielsen H, Minthon L, Janciauskiene S, Hansson O (2012) CCL2 is associated with a faster rate of cognitive decline during early stages of Alzheimer's disease. PLoS One 7, e30525.
16. Ishizuka K, Kimura T, Igata-yi R, Katsuragi S, Takamatsu J, Miyakawa T (1997) Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease. Psychiatry Clin Neurosci 51, 135-138. (Pubitemid 27262094)
17. Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, et al. (2004) Mild cognitive impairment-beyond controversies, towards a consensus: Report of the InternationalWorking Group on Mild Cognitive Impairment. J Intern Med 256, 240-246. (Pubitemid 39222993)
18. Magaki S, Mueller C, Dickson C, KirschW(2007) Increased production of inflammatory cytokines in mild cognitive impairment. Exp Gerontol 42, 233-240. (Pubitemid 46127771)
19. Selkoe DJ (1989) Amyloid beta protein precursor and the pathogenesis of Alzheimer's disease. Cell 58, 611-612. (Pubitemid 19210954)
20. Pike CJ, Burdick D,Walencewicz AJ, Glabe CG, CotmanCW (1993) Neurodegeneration induced by beta-amyloid peptides in vitro: The role of peptide assembly state. J Neurosci 13, 1676-1687. (Pubitemid 23095409)
21. Gruden MA, Davidova TB, Malisauskas M, Sewell RD, Voskresenskaya NI, Wilhelm K, Elistratova EI, Sherstnev VV, Morozova-Roche LA (2007) Differential neuroimmune markers to the onset of Alzheimer's disease neurodegeneration and dementia: Autoantibodies to A25-35 oligomers, S100 and neurotransmitters. J Neuroimmunol 186, 181-192. (Pubitemid 46773048)
22. Zoja C, Corna G, Morigi M, Donarelli R, Guglielmotti A, Pinza M et al. (1998) Bindarit retards renal disease and prolongs survival in murine lupus autoimmune disease. Kidney Int 53, 726-734. (Pubitemid 28124289)
23. Guglielmotti A, D'Onofrio E, Coletta I, Aquilini L, Milanese C, Pinza M (2002) Amelioration of rat adjuvant arthritis by therapeutic treatment with bindarit, an inhibitor of MCP-1 and TNF-a production. Inflamm Res 51, 252-258. (Pubitemid 34526441)
24. Bhatia M, Ramnath RD, Chevali L, Guglielmotti A (2005) Treatment with bindarit, a blocker of MCP-1 synthesis, protects mice against acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 288, G1259-G1265. (Pubitemid 40741080)
25. Bhatia M, Landolfi C, Basta F, Bovi G, Ramnath RD, de Joannon AC, Guglielmotti A (2008) Treatment with bindarit, an inhibitor of MCP-1 synthesis, protects mice against trinitrobenzene sulfonic acid-induced colitis. Inflamm Res 57, 464-471.
26. Rulli NE, Rolph MS, Srikiatkhachorn A, Anantapreecha S, Guglielmotti A, Mahalingam S (2011) Protection from arthritis and myositis in a mouse model of acute chikungunya virus disease by bindarit, an inhibitor of monocyte chemotactic protein-1 synthesis. J Infect Dis 204, 1026-1030.
27. Ge S, Shrestha B, Paul D, Keating C, Cone R, Guglielmotti A, Pachter JS (2012) The CCL2 synthesis inhibitor bindarit targets cells of the neurovascular unit, and suppresses experimental autoimmune encephalomyelitis. J Neuroinflammation 9, 171.
28. Culmsee C, Gerling N, Lehmann M, Nikolova-Karakashian M, Prehn JH, Mattson MP, Krieglstein J (2002) Nerve growth factor survival signaling in cultured hippocampal neurons is mediated through TrkA and requires the common neurotrophin receptor P75. Neuroscience 115, 1089-1108. (Pubitemid 35351700)
29. Volont́e C, Ciotti MT, Battistini L (1994) Development of a method for measuring cell number: Application to CNS primary neuronal cultures. Cytometry 17, 274-276.
30. Pieri M, Amadoro G, Carunchio I, Ciotti MT, Quaresima S, Florenzano F, Calissano P, Possenti R, Zona C, Severini C (2010) SP protects cerebellar granule cells against betaamyloid-induced apoptosis by down-regulation and reduced activity of Kv4 potassium channels. Neuropharmacology 58, 268-276.
31. Mirolo M, Fabbri M, Sironi M, Vecchi A, Guglielmotti A, Mangano G, Biondi G, Locati M, Mantovani (2008) Impact of the anti-inflammatory agent bindarit on the chemokinome: Selective inhibition of the monocyte chemotactic proteins. Eur Cytokine Netw 19, 119-122.
32. Mirzadegan T, Diehl F, Ebi B, Bhakta S, Polsky I, McCarley D, Mulkins M, Weatherhead GS, Lapierr JM, Dankwardt J, Morgans D Jr,Wilhelm R, Jarnagin K (2000) Identification of the binding site for a novel class of CCR2b chemokine receptor antagonists: Binding to a common chemokine receptor motif within the helical bundle. J Biol Chem 275, 25562-25571.
33. Johnstone M, Gearing AJ, Miller KM (1999) A central role for astrocytes in the inflammatory response to beta amyloid; chemokines, cytokines and reactive oxygen species are produced. J Neuroimmunol 93, 182-193. (Pubitemid 29051564)
34. Katayama T, Ito M, Kaneko S, Satoh M, Uehara T, MinamiM (2009) Reciprocal regulation of ATPgammaS-induced monocyte chemoattractant protein-1 production by ERK and p38 MAP kinases in rat corticostriatal slice cultures. J Neurosci Res 87, 1573-1581.
35. PanenkaW, Jijon H, Herx LM, Armstrong JN, Feighan D,Wei T, Yong VW, Ransohoff RM, MacVicar BA (2001) P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogenactivated protein kinase. J Neurosci 21, 7135-7142. (Pubitemid 32846961)
36. Town T, Nikolic V, Tan J (2005) The microglial "activation" continuum: From innate to adaptive responses. J Neuroinflammation 2, 24.
37. Dickson DW, Farlo J, Davies P, Crystal H, Fuld P, Yen SHC (1998) Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. Am J Pathol 132, 86-101.
38. Rogers J, Luber-Narod J, Styren SD, Civin WH (1988) Expression of immune system-associated antigens by cells of the human central nervous system: Relationship to the pathology of Alzheimer's disease. Neurobiol Aging 9, 339-349. (Pubitemid 19262065)
39. Cacquevel M, Lebeurrier N, Ch́eenne S, Vivien D (2004) Cytokines in neuroinflammation and Alzheimer's disease. Curr Drug Targets 5, 529-534. (Pubitemid 39004427)
40. Finch CE, Morgan TE (2007) Systemic inflammation, infection, ApoE alleles, and Alzheimer disease: A position paper. Curr Alzheimer Res 4, 185-189. (Pubitemid 46562393)
41. Mora E, Guglielmotti A, Biondi G, Sassone-Corsi P (2012) Bindarit: An anti-inflammatory small molecule that modulates the NFB pathway. Cell Cycle 11, 159-169.
42. Grassia G, Maddaluno M, Guglielmotti A, Mangano G, Biondi G, Maffia P, Ialenti A (2009) The anti-inflammatory agent bindarit inhibits neointima formation in both rats and hyperlipidaemic mice. Cardiovasc Res 84, 485-493.
43. Lin J, Zhu X, Chade AR, Jordan KL, Lavi R, Daghini E, Gibson ME, Guglielmotti A, Lerman A, Lerman LO (2009) Monocyte chemoattractant proteins mediate myocardial microvascular dysfunction in swine renovascular hypertension. Arterioscler Thromb Vasc Biol 30, e323.
44. Ble A, Mosca M, Di Loreto G, Guglielmotti A, Biondi G, Bombardieri S, Remuzzi G, Ruggenenti P (2011) Antiproteinuric effect of chemokine C-C motif ligand 2 inhibition in subjects with acute proliferative lupus nephritis.AmJ Nephrol 34, 367-372.
45. Smits HA, Rijsmus A, van Loon JH,Wat JW,Verhoef J, Boven LA, Nottet HS (2002) Amyloid-beta-induced chemokine production in primary human macrophages and astrocytes. J Neuroimmunol 127, 160-168. (Pubitemid 34603587)
46. Ḿelik-Parsadaniantz S, Rost̀ene W (2008) Chemokines and neuromodulation. J Neuroimmunol 198, 62-68.
47. Zhang ZJ, Dong YL, Lu Y, Cao S, Zhao ZQ, Gao YJ (2012) Chemokine CCL2 and its receptor CCR2 in the medullary dorsal horn are involved in trigeminal neuropathic pain. J Neuroinflammation 9, 136.
48. Old EA, Malcangio M (2012) Chemokine mediated neuronglia communication and aberrant signalling in neuropathic pain states. Curr Opin Pharmacol 12, 67-73.
49. Szczepanik AM, Funes S, PetkoW, Ringheim GE (2001) IL-4, IL-10 and IL-13 modulate A beta(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J Neuroimmunol 113, 49-62. (Pubitemid 32008670)
50. Szczepanik AM, Rampe D, Ringheim GE (2001) Amyloidbeta peptide fragments p3 and p4 induce pro-inflammatory cytokine and chemokine production in vitro and in vivo. J Neurochem 77, 304-317. (Pubitemid 32245104)
51. Kawamura M, Gachet C, Inoue K, Kato F (2004) Direct excitation of inhibitory interneurons by extracellular ATP mediated by P2Y1 receptors in the hippocampal slice. J Neurosci 24, 10835-10845. (Pubitemid 39602395)
52. Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7, 423-436. (Pubitemid 44012283)
53. Braun N, Zhu Y, Krieglstein J, Culmsee C, Zimmermann H (1998) Upregulation of the enzyme chain hydrolyzing extracellular ATP after transient forebrain ischemia in the rat. J Neurosci 18, 4891-4900. (Pubitemid 28285398)
54. Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR (1997) Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277, 813-817. (Pubitemid 27111317)
55. Chen ZP, Levy A, Lightman SL (2010) Nucleotides as extracellular signalling molecules. J Neuroendocrinol 7, 83-96.
56. Kong Q, Wang M, Liao Z, Camden JM, Yu S, Simonyi A, Sun GY, Gonzalez FA, Erb L, Seye CI, Weisman GA (2005) P2X(7) nucleotide receptors mediate caspase-8/9/3-dependent apoptosis in rat primary cortical neurons. Purinergic Signal 1, 337-347. (Pubitemid 43023767)
57. Barnard EA, Simon J, Webb TE (1997) Nucleotide receptors in the nervous system. An abundant component using diverse transduction mechanisms. Mol Neurobiol 15, 103-129.
58. Díaz-Herńandez M, Díez-Zaera M, Śanchez- Nogueiro J, Ǵomez-Villafuertes R, Canals JM, Alberch J, Miras-Portugal MT, Lucas JJ (2009) Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEBJ 23, 1893-1906.
59. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R (2003) 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. (Pubitemid 36800102)