Clemastine Confers Neuroprotection and Induces an Anti-Inflammatory Phenotype in SOD1G93A Mouse Model of Amyotrophic Lateral Sclerosis (original) (raw)

References

  1. Poppe L, Rue L, Robberecht W, Van Den Bosch L (2014) Translating biological findings into new treatment strategies for amyotrophic lateral sclerosis (ALS). Exp Neurol. doi:10.1016/j.expneurol.2014.07.001
  2. Andersen PM, Al-Chalabi A (2011) Clinical genetics of amyotrophic lateral sclerosis: what do we really know? Nat Rev Neurol 7(11):603–615
    Article CAS PubMed Google Scholar
  3. Philips T, Robberecht W (2011) Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol 10(3):253–263
    Article CAS PubMed Google Scholar
  4. Rizzo F, Riboldi G, Salani S, Nizzardo M, Simone C, Corti S, Hedlund E (2014) Cellular therapy to target neuroinflammation in amyotrophic lateral sclerosis. Cell Mol Life Sci 71(6):999–1015
    Article CAS PubMed Google Scholar
  5. Philips T, Rothstein JD (2014) Glial cells in amyotrophic lateral sclerosis. Exp Neurol. doi:10.1016/j.expneurol.2014.05.015
  6. Passani MB, Blandina P (2011) Histamine receptors in the CNS as targets for therapeutic intervention. Trends Pharmacol Sci 32(4):242–249
    Article CAS PubMed Google Scholar
  7. Provensi G, Coccurello R, Umehara H, Munari L, Giacovazzo G, Galeotti N, Nosi D, Gaetani S, Romano A, Moles A, Blandina P, Passani MB (2014) Satiety factor oleoylethanolamide recruits the brain histaminergic system to inhibit food intake. Proc Natl Acad Sci U S A 111(31):11527–11532
    Article CAS PubMed PubMed Central Google Scholar
  8. Passani MB, Ballerini C (2012) Histamine and neuroinflammation: insights from murine experimental autoimmune encephalomyelitis. Front Syst Neurosci 6:32
    Article CAS PubMed PubMed Central Google Scholar
  9. Saligrama N, Noubade R, Case LK, del Rio R, Teuscher C (2012) Combinatorial roles for histamine H1-H2 and H3-H4 receptors in autoimmune inflammatory disease of the central nervous system. Eur J Immunol 42(6):1536–1546
    Article CAS PubMed PubMed Central Google Scholar
  10. Katoh Y, Niimi M, Yamamoto Y, Kawamura T, Morimoto-Ishizuka T, Sawada M, Takemori H, Yamatodani A (2001) Histamine production by cultured microglial cells of the mouse. Neurosci Lett 305(3):181–184
    Article CAS PubMed Google Scholar
  11. Vizuete ML, Merino M, Venero JL, Santiago M, Cano J, Machado A (2000) Histamine infusion induces a selective dopaminergic neuronal death along with an inflammatory reaction in rat substantia nigra. J Neurochem 75(2):540–552
    Article CAS PubMed Google Scholar
  12. Hiraga N, Adachi N, Liu K, Nagaro T, Arai T (2007) Suppression of inflammatory cell recruitment by histamine receptor stimulation in ischemic rat brains. Eur J Pharmacol 557(2–3):236–244
    Article CAS PubMed Google Scholar
  13. Ferreira R, Santos T, Goncalves J, Baltazar G, Ferreira L, Agasse F, Bernardino L (2012) Histamine modulates microglia function. J Neuroinflammation 9:90
    Article PubMed PubMed Central Google Scholar
  14. Dong H, Zhang W, Zeng X, Hu G, Zhang H, He S, Zhang S (2014) Histamine induces upregulated expression of histamine receptors and increases release of inflammatory mediators from microglia. Mol Neurobiol 49(3):1487–1500
    Article CAS PubMed Google Scholar
  15. Zhu J, Qu C, Lu X, Zhang S (2014) Activation of microglia by histamine and substance P. Cell Physiol Biochem 34(3):768–780
    Article CAS PubMed Google Scholar
  16. Rocha SM, Pires J, Esteves M, Graca B, Bernardino L (2014) Histamine: a new immunomodulatory player in the neuron-glia crosstalk. Front Cell Neurosci 8:120
    Article PubMed PubMed Central Google Scholar
  17. Norenberg W, Hempel C, Urban N, Sobottka H, Illes P, Schaefer M (2011) Clemastine potentiates the human P2X7 receptor by sensitizing it to lower ATP concentrations. J Biol Chem 286(13):11067–11081
    Article PubMed PubMed Central Google Scholar
  18. Mei F, Fancy SP, Shen YA, Niu J, Zhao C, Presley B, Miao E, Lee S, Mayoral SR, Redmond SA, Etxeberria A, Xiao L, Franklin RJ, Green A, Hauser SL, Chan JR (2014) Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis. Nat Med 20(8):954–960
    Article CAS PubMed PubMed Central Google Scholar
  19. Johansen P, Weiss A, Bunter A, Waeckerle-Men Y, Fettelschoss A, Odermatt B, Kundig TM (2011) Clemastine causes immune suppression through inhibition of extracellular signal-regulated kinase-dependent proinflammatory cytokines. J Allergy Clin Immunol 128(6):1286–1294
    Article CAS PubMed Google Scholar
  20. Pizzasegola C, Caron I, Daleno C, Ronchi A, Minoia C, Carri MT, Bendotti C (2009) Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice. Amyotroph Lateral Scler 10(4):221–228
    Article CAS PubMed Google Scholar
  21. Apolloni S, Amadio S, Montilli C, Volonté C, D’Ambrosi N (2013) Ablation of P2X7 receptor exacerbates gliosis and motoneuron death in the SOD1-G93A mouse model of amyotrophic lateral sclerosis. Hum Mol Genet 22(20):4102–4116
    Article CAS PubMed Google Scholar
  22. Gapeyev ABSJ, Lushnikov KV, Chemeris NK (2006) Anti-inflammatory effects of low-intensity millimeter wave radiation. Bioelectromagnetics. Springer, Dordrecht
    Google Scholar
  23. Ludolph AC, Bendotti C, Blaugrund E, Chio A, Greensmith L, Loeffler JP, Mead R, Niessen HG, Petri S, Pradat PF, Robberecht W, Ruegg M, Schwalenstocker B, Stiller D, van den Berg L, Vieira F, von Horsten S (2010) Guidelines for preclinical animal research in ALS/MND: A consensus meeting. Amyotroph Lateral Scler 11(1–2):38–45
    Article PubMed Google Scholar
  24. Weydt P, Hong SY, Kliot M, Moller T (2003) Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport 14(7):1051–1054
    Article PubMed Google Scholar
  25. Thau N, Jungnickel J, Knippenberg S, Ratzka A, Dengler R, Petri S, Grothe C (2012) Prolonged survival and milder impairment of motor function in the SOD1 ALS mouse model devoid of fibroblast growth factor 2. Neurobiol Dis 47(2):248–257
    Article CAS PubMed Google Scholar
  26. Apolloni S, Parisi C, Pesaresi MG, Rossi S, Carri MT, Cozzolino M, Volonté C, D’Ambrosi N (2013) The NADPH oxidase pathway is dysregulated by the P2X7 receptor in the SOD1-G93A microglia model of amyotrophic lateral sclerosis. J Immunol 190(10):5187–5195
    Article CAS PubMed Google Scholar
  27. Nikodemova M, Small AL, Smith SM, Mitchell GS, Watters JJ (2014) Spinal but not cortical microglia acquire an atypical phenotype with high VEGF, galectin-3 and osteopontin, and blunted inflammatory responses in ALS rats. Neurobiol Dis 69:43–53
    Article CAS PubMed Google Scholar
  28. Chhor V, Le Charpentier T, Lebon S, Ore MV, Celador IL, Josserand J, Degos V, Jacotot E, Hagberg H, Savman K, Mallard C, Gressens P, Fleiss B (2013) Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav Immun 32:70–85
    Article CAS PubMed PubMed Central Google Scholar
  29. De Simone R, Niturad CE, De Nuccio C, Ajmone-Cat MA, Visentin S, Minghetti L (2010) TGF-beta and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J Neurochem 115(2):450–459
    Article PubMed Google Scholar
  30. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9(12):1512–1519
    Article CAS PubMed Google Scholar
  31. Fiala M, Chattopadhay M, La Cava A, Tse E, Liu G, Lourenco E, Eskin A, Liu PT, Magpantay L, Tse S, Mahanian M, Weitzman R, Tong J, Nguyen C, Cho T, Koo P, Sayre J, Martinez-Maza O, Rosenthal MJ, Wiedau-Pazos M (2010) IL-17A is increased in the serum and in spinal cord CD8 and mast cells of ALS patients. J Neuroinflammation 7:76
    Article PubMed PubMed Central Google Scholar
  32. Graves MC, Fiala M, Dinglasan LA, Liu NQ, Sayre J, Chiappelli F, van Kooten C, Vinters HV (2004) Inflammation in amyotrophic lateral sclerosis spinal cord and brain is mediated by activated macrophages, mast cells and T cells. Amyotroph Lateral Scler Other Motor Neuron Disord 5(4):213–219
    Article CAS PubMed Google Scholar
  33. Mizwicki MT, Fiala M, Magpantay L, Aziz N, Sayre J, Liu G, Siani A, Chan D, Martinez-Maza O, Chattopadhyay M, La Cava A (2012) Tocilizumab attenuates inflammation in ALS patients through inhibition of IL6 receptor signaling. Am J Neurodegener Dis 1(3):305–315
    PubMed PubMed Central Google Scholar
  34. Skaper SD, Facci L, Giusti P (2013) Glia and mast cells as targets for palmitoylethanolamide, an anti-inflammatory and neuroprotective lipid mediator. Mol Neurobiol 48(2):340–352
    Article CAS PubMed Google Scholar
  35. Skaper SD, Giusti P, Facci L (2014) Microglia and mast cells: two tracks on the road to neuroinflammation. FASEB J 26(8):3103–3117
    Article Google Scholar
  36. Haas HL, Sergeeva OA, Selbach O (2008) Histamine in the nervous system. Physiol Rev 88(3):1183–1241
    Article CAS PubMed Google Scholar
  37. Henkel JS, Beers DR, Zhao W, Appel SH (2009) Microglia in ALS: the good, the bad, and the resting. J Neuroimmune Pharmacol 4(4):389–398
    Article PubMed Google Scholar
  38. Beers DR, Zhao W, Liao B, Kano O, Wang J, Huang A, Appel SH, Henkel JS (2011) Neuroinflammation modulates distinct regional and temporal clinical responses in ALS mice. Brain Behav Immun 25(5):1025–1035
    Article CAS PubMed Google Scholar
  39. Zhao W, Beers DR, Appel SH (2013) Immune-mediated mechanisms in the pathoprogression of amyotrophic lateral sclerosis. J Neuroimmune Pharmacol 8(4):888–899
    Article PubMed PubMed Central Google Scholar
  40. Apolloni S, Amadio S, Parisi C, Matteucci A, Potenza RL, Armida M, Popoli P, D’Ambrosi N, Volonté C (2014) Spinal cord pathology is ameliorated by P2X7 antagonism in a SOD1-mutant mouse model of amyotrophic lateral sclerosis. Dis Model Mech 7(9):1101–1109
    Article PubMed PubMed Central Google Scholar
  41. Weisman GA, Camden JM, Peterson TS, Ajit D, Woods LT, Erb L (2012) P2 receptors for extracellular nucleotides in the central nervous system: role of P2X7 and P2Y(2) receptor interactions in neuroinflammation. Mol Neurobiol 46(1):96–113
    Article CAS PubMed PubMed Central Google Scholar
  42. Marden JJ, Harraz MM, Williams AJ, Nelson K, Luo M, Paulson H, Engelhardt JF (2007) Redox modifier genes in amyotrophic lateral sclerosis in mice. J Clin Invest 117(10):2913–2919
    Article CAS PubMed PubMed Central Google Scholar
  43. Trumbull KA, McAllister D, Gandelman MM, Fung WY, Lew T, Brennan L, Lopez N, Morre J, Kalyanaraman B, Beckman JS (2012) Diapocynin and apocynin administration fails to significantly extend survival in G93A SOD1 ALS mice. Neurobiol Dis 45(1):137–144
    Article CAS PubMed Google Scholar
  44. Parone PA, Da Cruz S, Han JS, McAlonis-Downes M, Vetto AP, Lee SK, Tseng E, Cleveland DW (2013) Enhancing mitochondrial calcium buffering capacity reduces aggregation of misfolded SOD1 and motor neuron cell death without extending survival in mouse models of inherited amyotrophic lateral sclerosis. J Neurosci 33(11):4657–4671
    Article CAS PubMed PubMed Central Google Scholar
  45. Huang G, Lee X, Bian Y, Shao Z, Sheng G, Pepinsky RB, Mi S (2013) Death receptor 6 (DR6) antagonist antibody is neuroprotective in the mouse SOD1G93A model of amyotrophic lateral sclerosis. Cell Death Dis 4:e841
    Article CAS PubMed PubMed Central Google Scholar
  46. Rouaux C, Panteleeva I, Rene F, Gonzalez de Aguilar JL, Echaniz-Laguna A, Dupuis L, Menger Y, Boutillier AL, Loeffler JP (2007) Sodium valproate exerts neuroprotective effects in vivo through CREB-binding protein-dependent mechanisms but does not improve survival in an amyotrophic lateral sclerosis mouse model. J Neurosci 27(21):5535–5545
    Article CAS PubMed Google Scholar
  47. D’Ambrosi N, Finocchi P, Apolloni S, Cozzolino M, Ferri A, Padovano V, Pietrini G, Carri MT, Volonté C (2009) The proinflammatory action of microglial P2 receptors is enhanced in SOD1 models for amyotrophic lateral sclerosis. J Immunol 183(7):4648–4656
    Article PubMed Google Scholar
  48. Pantano F, Berti P, Guida FM, Perrone G, Vincenzi B, Amato MM, Righi D, Dell’aquila E, Graziano F, Catalano V, Caricato M, Rizzo S, Muda AO, Russo A, Tonini G, Santini D (2013) The role of macrophages polarization in predicting prognosis of radically resected gastric cancer patients. J Cell Mol Med 17(11):1415–1421
    Article CAS PubMed PubMed Central Google Scholar
  49. Amadio S, Parisi C, Montilli C, Carrubba AS, Apolloni S, Volonté C (2014) P2Y(12) receptor on the verge of a neuroinflammatory breakdown. Mediat Inflamm 2014:975849

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