Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2017 (2017), Article ID 1626204, 14 pages
https://doi.org/10.1155/2017/1626204
Research Article

The Astrocytic S100B Protein with Its Receptor RAGE Is Aberrantly Expressed in SOD1G93A Models, and Its Inhibition Decreases the Expression of Proinflammatory Genes

1Institute of Anatomy and Cell Biology, Università Cattolica del Sacro Cuore, Rome, Italy
2Institute of Physiology and Biochemistry, Faculty of Biology, University of Belgrade, Belgrade, Serbia
3Department of Biology, University of Rome “Tor Vergata”, Rome, Italy
4IRCCS San Raffaele Scientific Institute, Università Vita-Salute San Raffaele, Milan, Italy

Correspondence should be addressed to Nadia D’Ambrosi; ti.2amorinu@isorbmad.aidan and Fabrizio Michetti; ti.ttacinu@ittehcim.oizirbaf

Received 21 February 2017; Accepted 30 April 2017; Published 20 June 2017

Academic Editor: Thomas Möller

Copyright © 2017 Alessia Serrano 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. S. Boillee, C. Vande Velde, and D. W. Cleveland, “ALS: a disease of motor neurons and their nonneuronal neighbors,” Neuron, vol. 52, no. 1, pp. 39–59, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Yamanaka, S. Boillee, E. A. Roberts et al., “Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 21, pp. 7594–7599, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. S. H. Kang, Y. Li, M. Fukaya et al., “Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis,” Nature Neuroscience, vol. 16, no. 5, pp. 571–579, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Bataveljic, L. Nikolić, M. Milosević, N. Todorović, and P. R. Andjus, “Changes in the astrocytic aquaporin-4 and inwardly rectifying potassium channel expression in the brain of the amyotrophic lateral sclerosis SOD1(G93A) rat model,” Glia, vol. 60, no. 12, pp. 1991–2003, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. R. B. Kim, C. W. Irvin, K. R. Tilva, and C. S. Mitchell, “State of the field: an informatics-based systematic review of the SOD1-G93A amyotrophic lateral sclerosis transgenic mouse model,” Amyotrophic Lateral Sclerosis Frontotemporal Degeneration, vol. 17, no. 1-2, pp. 1–14, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Philips and J. D. Rothstein, “Glial cells in amyotrophic lateral sclerosis,” Experimental Neurology, vol. 262, Part B, pp. 111–120, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Rossi, “Astrocyte physiopathology: at the crossroads of intercellular networking, inflammation and cell death,” Progress in Neurobiology, vol. 130, pp. 86–120, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. F. P. Di Giorgio, M. A. Carrasco, M. C. Siao, T. Maniatis, and K. Eggan, “Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model,” Nature Neuroscience, vol. 10, no. 5, pp. 608–614, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. F. P. Di Giorgio, G. L. Boulting, S. Bobrowicz, and K. C. Eggan, “Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation,” Cell Stem Cell, vol. 3, no. 6, pp. 637–648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. A. M. Haidet-Phillips, M. E. Hester, C. J. Miranda et al., “Astrocytes from familial and sporadic ALS patients are toxic to motor neurons,” Nature Biotechnology, vol. 29, no. 9, pp. 824–828, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Meyer, L. Ferraiuolo, C. J. Miranda et al., “Direct conversion of patient fibroblasts demonstrates non-cell autonomous toxicity of astrocytes to motor neurons in familial and sporadic ALS,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 2, pp. 829–832, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Ferri, M. Nencini, S. Battistini et al., “Activity of protein phosphatase calcineurin is decreased in sporadic and familial amyotrophic lateral sclerosispatients,” Journal of Neurochemistry, vol. 90, no. 5, pp. 1237–1242, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Nagai, D. B. Re, T. Nagata et al., “Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons,” Nature Neuroscience, vol. 10, no. 5, pp. 615–622, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Thundyil and K. L. Lim, “DAMPs and neurodegeneration,” Ageing Research Reviews, vol. 24, Part A, pp. 17–28, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Michetti, V. Corvino, M. C. Geloso et al., “The S100B protein in biological fluids: more than a lifelong biomarker of brain distress,” Journal of Neurochemistry, vol. 120, no. 5, pp. 644–659, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Villarreal, R. X. Aviles Reyes, M. F. Angelo, A. G. Reines, and A. J. Ramos, “S100B alters neuronal survival and dendrite extension via RAGE-mediated NF-kappaB signaling,” Journal of Neurochemistry, vol. 117, no. 2, pp. 321–332, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Villarreal, R. Seoane, A. González Torres et al., “S100B protein activates a RAGE-dependent autocrine loop in astrocytes: implications for its role in the propagation of reactive gliosis,” Journal of Neurochemistry, vol. 131, no. 2, pp. 190–205, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. K. A. Sterenczak, I. Nolte, and H. Murua Escobar, “RAGE splicing variants in mammals,” Methods in Molecular Biology, vol. 963, pp. 265–276, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. Z. Cai, N. Liu, C. Wang et al., “Role of RAGE in Alzheimer’s disease,” Cellular and Molecular Neurobiology, vol. 36, no. 4, pp. 483–495, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Sathe, W. Maetzler, J. D. Lang et al., “S100B is increased in Parkinson’s disease and ablation protects against MPTP-induced toxicity through the RAGE and TNF-alpha pathway,” Brain, vol. 135, Part 11, pp. 3336–3347, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Kamo, H. Haebara, I. Akiguchi, M. Kameyama, H. Kimura, and P. L. McGeer, “A distinctive distribution of reactive astroglia in the precentral cortex in amyotrophic lateral sclerosis,” Acta Neuropathologica, vol. 74, no. 1, pp. 33–38, 1987. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Migheli, S. Cordera, C. Bendotti, C. Atzori, R. Piva, and D. Schiffer, “S-100beta protein is upregulated in astrocytes and motor neurons in the spinal cord of patients with amyotrophic lateral sclerosis,” Neuroscience Letters, vol. 261, no. 1-2, pp. 25–28, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. S. D. Sussmuth, A. D. Sperfeld, A. Hinz et al., “CSF glial markers correlate with survival in amyotrophic lateral sclerosis,” Neurology, vol. 74, no. 12, pp. 982–987, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Cifra, F. Nani, and A. Nistri, “Riluzole is a potent drug to protect neonatal rat hypoglossal motoneurons in vitro from excitotoxicity due to glutamate uptake block,” The European Journal of Neuroscience, vol. 33, no. 5, pp. 899–913, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Shobha, P. A. Alladi, A. Nalini, T. N. Sathyaprabha, and T. R. Raju, “Exposure to CSF from sporadic amyotrophic lateral sclerosis patients induces morphological transformation of astroglia and enhances GFAP and S100beta expression,” Neuroscience Letters, vol. 473, no. 1, pp. 56–61, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Diaz-Amarilla, S. Olivera-Bravo, E. Trias et al., “Phenotypically aberrant astrocytes that promote motoneuron damage in a model of inherited amyotrophic lateral sclerosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 44, pp. 18126–18131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Casula, A. M. Iyer, W. G. Spliet et al., “Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue,” Neuroscience, vol. 179, pp. 233–243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. J. K. Juranek, G. K. Daffu, J. Wojtkiewicz, D. Lacomis, J. Kofler, and A. M. Schmidt, “Receptor for advanced glycation end products and its inflammatory ligands are upregulated in amyotrophic lateral sclerosis,” Frontiers in Cellular Neuroscience, vol. 9, p. 485, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. D. S. Howland, J. Liu, Y. She et al., “Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS),” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 3, pp. 1604–1609, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Apolloni, S. Amadio, C. Montilli, C. Volonté, and N. D'Ambrosi, “Ablation of P2X7 receptor exacerbates gliosis and motoneuron death in the SOD1-G93A mouse model of amyotrophic lateral sclerosis,” Human Molecular Genetics, vol. 22, no. 20, pp. 4102–4116, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Mecha, P. M. Iñigo, L. Mestre, M. Hernangómez, J. Borrell, and C. Guaza, “An easy and fast way to obtain a high number of glial cells from rat cerebral tissue: a beginners approach,” Nature-Protocol Exchange, vol. 218, 2011. View at Publisher · View at Google Scholar
  32. G. M. Thomsen, G. Gowing, J. Latter et al., “Delayed disease onset and extended survival in the SOD1G93A rat model of amyotrophic lateral sclerosis after suppression of mutant SOD1 in the motor cortex,” The Journal of Neuroscience, vol. 34, no. 47, pp. 15587–15600, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Matsumoto, Y. Okada, M. Nakamichi et al., “Disease progression of human SOD1 (G93A) transgenic ALS model rats,” Journal of Neuroscience Research, vol. 83, no. 1, pp. 119–133, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. J. C. Tobon-Velasco, E. Cuevas, and M. A. Torres-Ramos, “Receptor for AGEs (RAGE) as mediator of NF-kB pathway activation in neuroinflammation and oxidative stress,” CNS & Neurological Disorders Drug Targets, vol. 13, no. 9, pp. 1615–1626, 2014. View at Publisher · View at Google Scholar
  35. A. Nonneman, W. Robberecht, and L. Van Den Bosch, “The role of oligodendroglial dysfunction in amyotrophic lateral sclerosis,” Neurodegenerative Disease Management, vol. 4, no. 3, pp. 223–239, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Trias, P. Díaz-Amarilla, S. Olivera-Bravo et al., “Phenotypic transition of microglia into astrocyte-like cells associated with disease onset in a model of inherited ALS,” Frontiers in Cellular Neuroscience, vol. 7, p. 274, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Kim, H. J. Waldvogel, R. L. Faull, M. A. Curtis, and L. F. Nicholson, “The RAGE receptor and its ligands are highly expressed in astrocytes in a grade-dependant manner in the striatum and subependymal layer in Huntington’s disease,” Journal of Neurochemistry, vol. 134, no. 5, pp. 927–942, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Roltsch, L. Holcomb, K. A. Young, A. Marks, and D. B. Zimmer, “PSAPP mice exhibit regionally selective reductions in gliosis and plaque deposition in response to S100B ablation,” Journal of Neuroinflammation, vol. 7, no. 1, p. 78, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Lee, S. J. Hyeon, H. Im, H. Ryu, Y. Kim, and H. Ryu, “Astrocytes and microglia as non-cell autonomous players in the pathogenesis of ALS,” Experimental Neurobiology, vol. 25, no. 5, pp. 233–240, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Philips and W. Robberecht, “Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease,” Lancet Neurology, vol. 10, no. 3, pp. 253–263, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. E. D. Hall, J. A. Oostveen, and M. E. Gurney, “Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS,” Glia, vol. 23, no. 3, pp. 249–256, 1998. View at Publisher · View at Google Scholar
  42. M. E. Alexianu, M. Kozovska, and S. H. Appel, “Immune reactivity in a mouse model of familial ALS correlates with disease progression,” Neurology, vol. 57, no. 7, pp. 1282–1289, 2001. View at Publisher · View at Google Scholar
  43. H. Kawamata, S. K. Ng, N. Diaz et al., “Abnormal intracellular calcium signaling and SNARE-dependent exocytosis contributes to SOD1G93A astrocyte-mediated toxicity in amyotrophic lateral sclerosis,” The Journal of Neuroscience, vol. 34, no. 6, pp. 2331–2348, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. P. L. Ferguson and G. S. Shaw, “Role of the N-terminal helix I for dimerization and stability of the calcium-binding protein S100B,” Biochemistry, vol. 41, no. 11, pp. 3637–3646, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Sun, Y. Sun, S. C. Ling et al., “Translational profiling identifies a cascade of damage initiated in motor neurons and spreading to glia in mutant SOD1-mediated ALS,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 50, pp. E6993–E7002, 2015. View at Publisher · View at Google Scholar · View at Scopus