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Mediators of Inflammation
Volume 2016, Article ID 1346390, 11 pages
http://dx.doi.org/10.1155/2016/1346390
Research Article

Epobis is a Nonerythropoietic and Neuroprotective Agonist of the Erythropoietin Receptor with Anti-Inflammatory and Memory Enhancing Effects

1Laboratory of Neural Plasticity, Department of Neuroscience and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
2Research Laboratory for Stereology and Neuroscience, Bispebjerg-Frederiksberg Hospital, Copenhagen University Hospital, Copenhagen, Denmark
3Juliane Marie Centret, Rigshospitalet (Copenhagen University Hospital), Copenhagen, Denmark

Received 2 May 2016; Revised 26 August 2016; Accepted 15 September 2016

Academic Editor: Mirella Giovarelli

Copyright © 2016 Oksana Dmytriyeva et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. F. Bunn, “Erythropoietin,” Cold Spring Harbor Perspectives in Medicine, vol. 3, no. 3, Article ID a011619, pp. 1–20, 2013. View at Publisher · View at Google Scholar
  2. K. Maiese, Z. Z. Chong, Y. C. Shang, and S. Wang, “Erythropoietin: new directions for the nervous system,” International Journal of Molecular Sciences, vol. 13, no. 9, pp. 11102–11129, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Subirós, D. G. Del Barco, and R. M. Coro-Antich, “Erythropoietin: still on the neuroprotection road,” Therapeutic Advances in Neurological Disorders, vol. 5, no. 3, pp. 161–173, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. W. Jang, J. Park, K. J. Shin et al., “Safety and efficacy of recombinant human erythropoietin treatment of non-motor symptoms in Parkinson's disease,” Journal of the Neurological Sciences, vol. 337, no. 1-2, pp. 47–54, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Créange, J.-P. Lefaucheur, M.-O. Balleyguier, and F. Galactéros, “Iron depletion induced by bloodletting and followed by rhEPO administration as a therapeutic strategy in progressive multiple sclerosis: a pilot, open-label study with neurophysiological measurements,” Neurophysiologie Clinique, vol. 43, no. 5-6, pp. 303–312, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Najmi Varzaneh, F. Najmi Varzaneh, A. R. Azimi, N. Rezaei, and M. A. Sahraian, “Efficacy of combination therapy with erythropoietin and methylprednisolone in clinical recovery of severe relapse in multiple sclerosis,” Acta Neurologica Belgica, vol. 114, no. 4, pp. 273–278, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Q. Nguyen, B. H. Cherry, G. F. Scott, M.-G. Ryou, and R. T. Mallet, “Erythropoietin: powerful protection of ischemic and post-ischemic brain,” Experimental Biology and Medicine, vol. 239, no. 11, pp. 1461–1475, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Pang, M. Bian, X.-X. Zang et al., “Neuroprotective effects of erythropoietin in patients with carbon monoxide poisoning,” Journal of Biochemical and Molecular Toxicology, vol. 27, no. 5, pp. 266–271, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. J. D. Turner, A. Mammis, and C. J. Prestigiacomo, “Erythropoietin for the treatment of subarachnoid hemorrhage: a review,” World Neurosurgery, vol. 73, no. 5, pp. 500–507, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Mariotti, W. Nachbauer, M. Panzeri, W. Poewe, F. Taroni, and S. Boesch, “Erythropoietin in Friedreich ataxia,” Journal of Neurochemistry, vol. 126, no. 1, pp. 80–87, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. K. W. Miskowiak, M. Vinberg, C. J. Harmer, H. Ehrenreich, and L. V. Kessing, “Erythropoietin: a candidate treatment for mood symptoms and memory dysfunction in depression,” Psychopharmacology, vol. 219, no. 3, pp. 687–698, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. S.-T. Lee, K. Chu, J.-E. Park et al., “Erythropoietin improves memory function with reducing endothelial dysfunction and amyloid-beta burden in Alzheimer's disease models,” Journal of Neurochemistry, vol. 120, no. 1, pp. 115–124, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Hamidi, Z. Arabpour, M. Shabrang et al., “Erythropoietin improves spatial learning and memory in streptozotocin model of dementia,” Pathophysiology, vol. 20, no. 2, pp. 153–158, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Maurice, M. H. Mustafa, C. Desrumaux et al., “Intranasal formulation of erythropoietin (EPO) showed potent protective activity against amyloid toxicity in the Aβ25–35 non-transgenic mouse model of Alzheimer's disease,” Journal of Psychopharmacology, vol. 27, no. 11, pp. 1044–1057, 2013. View at Publisher · View at Google Scholar
  15. X. Wei, Y. Li, X. Sun et al., “Erythropoietin protects against murine cerebral malaria through actions on host cellular immunity,” Infection and Immunity, vol. 82, no. 1, pp. 165–173, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Barichello, L. R. Simões, J. S. Generoso et al., “Erythropoietin prevents cognitive impairment and oxidative parameters in Wistar rats subjected to pneumococcal meningitis,” Translational Research, vol. 163, no. 5, pp. 503–513, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Y. Noh, K. A. Cho, H. Kim, S.-M. Kim, and S. H. Kim, “Erythropoietin modulates the immune-inflammatory response of a SOD1G93A transgenic mouse model of amyotrophic lateral sclerosis (ALS),” Neuroscience Letters, vol. 574, pp. 53–58, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Hines-Beard, S. Desai, R. Haag et al., “Identification of a therapeutic dose of continuously delivered erythropoietin in the eye using an inducible promoter system,” Current Gene Therapy, vol. 13, no. 4, pp. 275–281, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. Ş. Ç. Sözmen, S. H. Kurul, U. Yiş, K. Tuĝyan, B. Baykara, and O. Yilmaz, “Neuroprotective effects of recombinant human erythropoietin in the developing brain of rat after lithium-pilocarpine induced status epilepticus,” Brain and Development, vol. 34, no. 3, pp. 189–195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Ning, A. Zhang, H. Song et al., “Recombinant human erythropoietin prevents motor neuron apoptosis in a rat model of cervical sub-acute spinal cord compression,” Neuroscience Letters, vol. 490, no. 1, pp. 57–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. Q.-H. Zhou, R. J. Boado, J. Z. Lu, E. K.-W. Hui, and W. M. Pardridge, “Re-engineering erythropoietin as an IgG fusion protein that penetrates the blood-brain barrier in the mouse,” Molecular Pharmaceutics, vol. 7, no. 6, pp. 2148–2155, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Dhanushkodi, E. O. Akano, E. E. Roguski et al., “A single intramuscular injection of rAAV-mediated mutant erythropoietin protects against MPTP-induced parkinsonism,” Genes, Brain and Behavior, vol. 12, no. 2, pp. 224–233, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. J. C. G. Rodríguez and I. S. Teste, “The nasal route as a potential pathway for delivery of erythropoietin in the treatment of acute ischemic stroke in humans,” The Scientific World Journal, vol. 9, pp. 970–981, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Brines, N. S. A. Patel, P. Villa et al., “Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 31, pp. 10925–10930, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Chen, B. Luo, X. Yang et al., “Therapeutic effects of nonerythropoietic erythropoietin analog ARA290 in experimental autoimmune encephalomyelitis rat,” Journal of Neuroimmunology, vol. 268, no. 1-2, pp. 64–70, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Pankratova, D. Kiryushko, K. Sonn et al., “Neuroprotective properties of a novel, non-haematopoietic agonist of the erythropoietin receptor,” Brain, vol. 133, no. 8, pp. 2281–2294, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. S. Syed, S. W. Reid, C. Li et al., “Efficiency of signalling through cytokine receptors depends critically on receptor orientation,” Nature, vol. 395, no. 6701, pp. 511–516, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Zellinger, N. Seeger, M. Hadamitzky et al., “Impact of the erythropoietin-derived peptide mimetic Epotris on the histopathological consequences of status epilepticus,” Epilepsy Research, vol. 96, no. 3, pp. 241–249, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Pankratova, B. Gu, D. Kiryushko et al., “A new agonist of the erythropoietin receptor, Epobis, induces neurite outgrowth and promotes neuronal survival,” Journal of Neurochemistry, vol. 121, no. 6, pp. 915–923, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Moldovan, V. Pinchenko, O. Dmytriyeva et al., “Peptide mimetic of the S100A4 protein modulates peripheral nerve regeneration and attenuates the progression of neuropathy in myelin protein P0 null mice,” Molecular Medicine, vol. 19, no. 1, pp. 43–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. D. A. Flick and G. E. Gifford, “Comparison of in vitro cell cytotoxic assays for tumor necrosis factor,” Journal of Immunological Methods, vol. 68, no. 1-2, pp. 167–175, 1984. View at Publisher · View at Google Scholar · View at Scopus
  32. M. N. Enevoldsen, A. Kochoyan, M. Jurgenson et al., “Neuroprotective and memory enhancing properties of a dual agonist of the FGF receptor and NCAM,” Neurobiology of Disease, vol. 48, no. 3, pp. 533–545, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Klementiev, S. Li, I. Korshunova et al., “Anti-inflammatory properties of a novel peptide interleukin 1 receptor antagonist,” Journal of Neuroinflammation, vol. 11, no. 1, article 27, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. L. K. Ryan, D. T. Golenbock, J. Wu, and M. W. Vermeulen, “Characterization of proinflammatory cytokine production and CD14 expression by murine alveolar macrophage cell lines,” In Vitro Cellular & Developmental Biology—Animal, vol. 33, no. 8, pp. 647–653, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. O. Butovsky, A. E. Talpalar, K. Ben-Yaakov, and M. Schwartz, “Activation of microglia by aggregated β-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-γ and IL-4 render them protective,” Molecular and Cellular Neuroscience, vol. 29, no. 3, pp. 381–393, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Secher, V. Novitskaia, V. Berezin, E. Bock, B. Glenthøj, and B. Klementiev, “A neural cell adhesion molecule-derived fibroblast growth factor receptor agonist, the FGL-peptide, promotes early postnatal sensorimotor development and enhances social memory retention,” Neuroscience, vol. 141, no. 3, pp. 1289–1299, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. J. R. Mathiasen and A. DiCamillo, “Social recognition assay in the rat,” in Current Protocols in Neuroscience, UNIT 8.5I, pp. 1–15, John Wiley & Sons, New York, NY, USA, 2010. View at Publisher · View at Google Scholar
  38. B. Klementiev, T. Novikova, V. Novitskaya et al., “A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Aβ25-35,” Neuroscience, vol. 145, no. 1, pp. 209–224, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Gotfryd, S. Owczarek, K. Hoffmann et al., “Multiple effects of pentyl-4-yn-VPA enantiomers: from toxicity to short-term memory enhancement,” Neuropharmacology, vol. 52, no. 3, pp. 764–778, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Adamcio, D. Sargin, A. Stradomska et al., “Erythropoietin enhances hippocampal long-term potentiation and memory,” BMC Biology, vol. 6, article 37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. W. M. Campana, X. Li, V. I. Shubayev, M. Angert, K. Cai, and R. R. Myers, “Erythropoietin reduces Schwann cell TNF-α, Wallerian degeneration and pain-related behaviors after peripheral nerve injury,” The European Journal of Neuroscience, vol. 23, no. 3, pp. 617–626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Yazihan, O. Karakurt, and H. Ataoglu, “Erythropoietin reduces lipopolysaccharide-induced cell Damage and midkine secretion in U937 human histiocytic lymphoma cells,” Advances in Therapy, vol. 25, no. 5, pp. 502–514, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Brines and A. Cerami, “Emerging biological roles for erythropoietin in the nervous system,” Nature Reviews Neuroscience, vol. 6, no. 6, pp. 484–494, 2005. View at Google Scholar · View at Scopus
  44. D. Agnello, P. Bigini, P. Villa et al., “Erythropoietin exerts an anti-inflammatory effect on the CNS in a model of experimental autoimmune encephalomyelitis,” Brain Research, vol. 952, no. 1, pp. 128–134, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Villa, P. Bigini, T. Mennini et al., “Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis,” The Journal of Experimental Medicine, vol. 198, no. 6, pp. 971–975, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Shin, M. Ahn, C. Moon, and S. Kim, “Erythropoietin and autoimmune neuroinflammation: lessons from experimental autoimmune encephalomyelitis and experimental autoimmune neuritis,” Anatomy & Cell Biology, vol. 45, no. 4, pp. 215–220, 2012. View at Publisher · View at Google Scholar
  47. I. Cervellini, P. Ghezzi, and M. Mengozzi, “Therapeutic efficacy of erythrpoietin in experimental autoimmune encephalomyelitis in mice, a model of multiple sclerosis,” Methods in Molecular Biology, vol. 982, pp. 163–173, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. S.-J. Chen, Y.-L. Wang, W.-T. Lo et al., “Erythropoietin enhances endogenous haem oxygenase-1 and represses immune responses to ameliorate experimental autoimmune encephalomyelitis,” Clinical and Experimental Immunology, vol. 162, no. 2, pp. 210–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. S.-Y. Kang, J.-H. Kang, J. C. Choi, J. S. Lee, C. S. Lee, and T. Shin, “Expression of erythropoietin in the spinal cord of lewis rats with experimental autoimmune encephalomyelitis,” Journal of Clinical Neurology, vol. 5, no. 1, pp. 39–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. C. S. Robertson, R. Garcia, S. S. K. Gaddam et al., “Treatment of mild traumatic brain injury with an erythropoietin-mimetic peptide,” Journal of Neurotrauma, vol. 30, no. 9, pp. 765–774, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. M. E. Schober, D. F. Requena, B. Block et al., “Erythropoietin improved cognitive function and decreased hippocampal caspase activity in rat pups after traumatic brain injury,” Journal of Neurotrauma, vol. 31, no. 4, pp. 358–369, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. M. Al-Qahtani, B. A. Abdel-Wahab, and S. M. Abd El-Aziz, “Long-term moderate dose exogenous erythropoietin treatment protects from intermittent hypoxia-induced spatial learning deficits and hippocampal oxidative stress in young rats,” Neurochemical Research, vol. 39, no. 1, pp. 161–171, 2014. View at Publisher · View at Google Scholar · View at Scopus