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Mediators of Inflammation
Volume 2018, Article ID 7219732, 11 pages
https://doi.org/10.1155/2018/7219732
Review Article

Impact of Aging in Microglia-Mediated D-Serine Balance in the CNS

1Departamento de Neurología, Escuela de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
2Departamento de Biología, Facultad de Química y Biología, Universidad de Santiago de Chile, Santiago, Chile

Correspondence should be addressed to Jaime Eugenín; lc.hcasu@ninegue.emiaj and Rommy von Bernhardi; lc.cup.dem@bnovr

Received 9 June 2018; Revised 19 August 2018; Accepted 30 August 2018; Published 27 September 2018

Academic Editor: Marcella Reale

Copyright © 2018 Sebastián Beltrán-Castillo 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. Pawate, Q. Shen, F. Fan, and N. R. Bhat, “Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma,” Journal of Neuroscience Research, vol. 77, no. 4, pp. 540–551, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Qin, G. Li, X. Qian et al., “Interactive role of the toll-like receptor 4 and reactive oxygen species in LPS-induced microglia activation,” Glia, vol. 52, no. 1, pp. 78–84, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Hayashi, M. Yoshida, M. Yamato et al., “Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor A in mice,” The Journal of Neuroscience, vol. 28, no. 34, pp. 8624–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. W. Gomes-Leal, “Microglial physiopathology: how to explain the dual role of microglia after acute neural disorders?” Brain and Behavior: A Cognitive Neuroscience Perspective, vol. 2, no. 3, pp. 345–356, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J. P. Mothet, A. T. Parent, H. Wolosker et al., “D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4926–4931, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. M. J. Schell, M. E. Molliver, and S. H. Snyder, “D-serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 9, pp. 3948–3952, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Z. Wu, A. M. Bodles, M. M. Porter, W. S. Griffin, A. S. Basile, and S. W. Barger, “Induction of serine racemase expression and D-serine release from microglia by amyloid β-peptide,” Journal of Neuroinflammation, vol. 1, no. 1, p. 2, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. S. M. Williams, C. M. Diaz, L. T. Macnab, R. K. Sullivan, and D. V. Pow, “Immunocytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons,” Glia, vol. 53, no. 4, pp. 401–411, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Wolosker, E. Dumin, L. Balan, and V. N. Foltyn, “D-amino acids in the brain: D-serine in neurotransmission and neurodegeneration,” The FEBS Journal, vol. 275, no. 14, pp. 3514–3526, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Ding, N. Ma, M. Nagahama, K. Yamada, and R. Semba, “Localization of D-serine and serine racemase in neurons and neuroglias in mouse brain,” Neurological Sciences, vol. 32, no. 2, pp. 263–267, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Beltran-Castillo, M. J. Olivares, R. A. Contreras et al., “D-serine released by astrocytes in brainstem regulates breathing response to CO2 levels,” Nature Communications, vol. 8, no. 1, p. 838, 2017. View at Publisher · View at Google Scholar · View at Scopus
  12. R. von Bernhardi, L. Eugenin-von Bernhardi, and J. Eugenin, “Microglial cell dysregulation in brain aging and neurodegeneration,” Frontiers in Aging Neuroscience, vol. 7, p. 124, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. W. J. Streit, N. W. Sammons, A. J. Kuhns, and D. L. Sparks, “Dystrophic microglia in the aging human brain,” Glia, vol. 45, no. 2, pp. 208–212, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. S. M. Ye and R. W. Johnson, “Increased interleukin-6 expression by microglia from brain of aged mice,” Journal of Neuroimmunology, vol. 93, no. 1-2, pp. 139–148, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Sierra, A. C. Gottfried-Blackmore, B. S. McEwen, and K. Bulloch, “Microglia derived from aging mice exhibit an altered inflammatory profile,” Glia, vol. 55, no. 4, pp. 412–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. J. E. Tichauer and R. von Bernhardi, “Transforming growth factor-β stimulates β amyloid uptake by microglia through Smad3-dependent mechanisms,” Journal of Neuroscience Research, vol. 90, no. 10, pp. 1970–1980, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. A. M. Floden and C. K. Combs, “Microglia demonstrate age-dependent interaction with amyloid-β fibrils,” Journal of Alzheimer's Disease, vol. 25, no. 2, pp. 279–293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. R. von Bernhardi, J. Tichauer, and L. Eugenin-von Bernhardi, “Proliferating culture of aged microglia for the study of neurodegenerative diseases,” Journal of Neuroscience Methods, vol. 202, no. 1, pp. 65–69, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J. E. Tichauer, B. Flores, B. Soler, L. Eugenin-von Bernhardi, G. Ramirez, and R. von Bernhardi, “Age-dependent changes on TGFβ1 Smad3 pathway modify the pattern of microglial cell activation,” Brain, Behavior, and Immunity, vol. 37, pp. 187–196, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. N. W. Kleckner and R. Dingledine, “Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes,” Science, vol. 241, no. 4867, pp. 835–837, 1988. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Hashimoto, T. Nishikawa, T. Hayashi et al., “The presence of free D-serine in rat brain,” FEBS Letters, vol. 296, no. 1, pp. 33–36, 1992. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. Schell, R. O. Brady, Jr, M. E. Molliver, and S. H. Snyder, “D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors,” The Journal of Neuroscience, vol. 17, no. 5, pp. 1604–1615, 1997. View at Publisher · View at Google Scholar
  23. A. Hashimoto, T. Nishikawa, T. Oka, and K. Takahashi, “Endogenous D-serine in rat brain: N-methyl-D-aspartate receptor-related distribution and aging,” Journal of Neurochemistry, vol. 60, no. 2, pp. 783–786, 1993. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Wolosker, S. Blackshaw, and S. H. Snyder, “Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 23, pp. 13409–13414, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Wolosker, K. N. Sheth, M. Takahashi et al., “Purification of serine racemase: biosynthesis of the neuromodulator D-serine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 2, pp. 721–725, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. V. N. Foltyn, I. Bendikov, J. De Miranda et al., “Serine racemase modulates intracellular D-serine levels through an alpha, beta-elimination activity,” The Journal of Biological Chemistry, vol. 280, no. 3, pp. 1754–1763, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Nagata, “Involvement of D-amino acid oxidase in elimination of D-serine in mouse brain,” Experientia, vol. 48, no. 8, pp. 753–755, 1992. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Miya, R. Inoue, Y. Takata et al., “Serine racemase is predominantly localized in neurons in mouse brain,” The Journal of Comparative Neurology, vol. 510, no. 6, pp. 641–654, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Puyal, M. Martineau, J. P. Mothet, M. T. Nicolas, and J. Raymond, “Changes in D-serine levels and localization during postnatal development of the rat vestibular nuclei,” The Journal of Comparative Neurology, vol. 497, no. 4, pp. 610–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Dun, J. Duplantier, P. Roon, P. M. Martin, V. Ganapathy, and S. B. Smith, “Serine racemase expression and D-serine content are developmentally regulated in neuronal ganglion cells of the retina,” Journal of Neurochemistry, vol. 104, no. 4, pp. 970–978, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. E. R. Stevens, M. Esguerra, P. M. Kim et al., “D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 11, pp. 6789–6794, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Papouin, C. Henneberger, D. A. Rusakov, and S. H. R. Oliet, “Astroglial versus neuronal D-serine: fact checking,” Trends in Neurosciences, vol. 40, no. 9, pp. 517–520, 2017. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Wolosker, D. T. Balu, and J. T. Coyle, “Astroglial versus neuronal D-serine: check your controls!,” Trends in Neurosciences, vol. 40, no. 9, pp. 520–522, 2017. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Wu and S. W. Barger, “Induction of serine racemase by inflammatory stimuli is dependent on AP-1,” Annals of the New York Academy of Sciences, vol. 1035, no. 1, pp. 133–146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Wu, A. S. Basile, and S. W. Barger, “Induction of serine racemase expression and D-serine release from microglia by secreted amyloid precursor protein (sAPP),” Current Alzheimer Research, vol. 4, no. 3, pp. 243–251, 2007. View at Google Scholar
  36. M. Yamasaki, K. Yamada, S. Furuya, J. Mitoma, Y. Hirabayashi, and M. Watanabe, “3-Phosphoglycerate dehydrogenase, a key enzyme for l-serine biosynthesis, is preferentially expressed in the radial glia/astrocyte lineage and olfactory ensheathing glia in the mouse brain,” The Journal of Neuroscience, vol. 21, no. 19, pp. 7691–7704, 2001. View at Publisher · View at Google Scholar
  37. J. H. Yang, A. Wada, K. Yoshida et al., “Brain-specific Phgdh deletion reveals a pivotal role for L-serine biosynthesis in controlling the level of D-serine, an N-methyl-D-aspartate receptor co-agonist, in adult brain,” The Journal of Biological Chemistry, vol. 285, no. 53, pp. 41380–41390, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. J. T. Ehmsen, T. M. Ma, H. Sason et al., “D-serine in glia and neurons derives from 3-phosphoglycerate dehydrogenase,” The Journal of Neuroscience, vol. 33, no. 30, pp. 12464–12469, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Wolosker, “Serine racemase and the serine shuttle between neurons and astrocytes,” Biochimica et Biophysica Acta, vol. 1814, no. 11, pp. 1558–1566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. C. S. Ribeiro, M. Reis, R. Panizzutti, J. de Miranda, and H. Wolosker, “Glial transport of the neuromodulator D-serine,” Brain Research, vol. 929, no. 2, pp. 202–209, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. J. P. Mothet, L. Pollegioni, G. Ouanounou, M. Martineau, P. Fossier, and G. Baux, “Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 15, pp. 5606–5611, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Henneberger, T. Papouin, S. H. Oliet, and D. A. Rusakov, “Long-term potentiation depends on release of D-serine from astrocytes,” Nature, vol. 463, no. 7278, pp. 232–236, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Rosenberg, E. Kartvelishvily, M. Shleper, C. M. Klinker, M. T. Bowser, and H. Wolosker, “Neuronal release of D-serine: a physiological pathway controlling extracellular D-serine concentration,” The FASEB Journal, vol. 24, no. 8, pp. 2951–2961, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Takata, T. Mishima, C. Hisatsune et al., “Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo,” The Journal of Neuroscience, vol. 31, no. 49, pp. 18155–18165, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Stehberg, R. Moraga-Amaro, C. Salazar et al., “Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala,” The FASEB Journal, vol. 26, no. 9, pp. 3649–3657, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Maucler, P. Pernot, N. Vasylieva, L. Pollegioni, and S. Marinesco, “In vivo D-serine hetero-exchange through alanine-serine-cysteine (ASC) transporters detected by microelectrode biosensors,” ACS Chemical Neuroscience, vol. 4, no. 5, pp. 772–781, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Shigetomi, O. Jackson-Weaver, R. T. Huckstepp, T. J. O'Dell, and B. S. Khakh, “TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release,” The Journal of Neuroscience, vol. 33, no. 24, pp. 10143–10153, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Martineau, V. Parpura, and J. P. Mothet, “Cell-type specific mechanisms of D-serine uptake and release in the brain,” Frontiers in Synaptic Neuroscience, vol. 6, p. 12, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Junjaud, E. Rouaud, F. Turpin, J. P. Mothet, and J. M. Billard, “Age-related effects of the neuromodulator D-serine on neurotransmission and synaptic potentiation in the CA1 hippocampal area of the rat,” Journal of Neurochemistry, vol. 98, no. 4, pp. 1159–1166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. L. P. Diniz, J. C. Almeida, V. Tortelli et al., “Astrocyte-induced synaptogenesis is mediated by transforming growth factor β signaling through modulation of D-serine levels in cerebral cortex neurons,” Journal of Biological Chemistry, vol. 287, no. 49, pp. 41432–41445, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. R. D. Steinmetz, E. Fava, P. Nicotera, and D. Steinhilber, “A simple cell line based in vitro test system for N-methyl-D-aspartate (NMDA) receptor ligands,” Journal of Neuroscience Methods, vol. 113, no. 1, pp. 99–110, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Katsuki, Y. Watanabe, S. Fujimoto, T. Kume, and A. Akaike, “Contribution of endogenous glycine and d-serine to excitotoxic and ischemic cell death in rat cerebrocortical slice cultures,” Life Sciences, vol. 81, no. 9, pp. 740–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. J. M. Billard, “D-serine in the aging hippocampus,” Journal of Pharmaceutical and Biomedical Analysis, vol. 116, pp. 18–24, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. W. J. Streit, “Microglia as neuroprotective, immunocompetent cells of the CNS,” Glia, vol. 40, no. 2, pp. 133–139, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Kettenmann, U. K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, no. 2, pp. 461–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. R. von Bernhardi and J. Eugenin, “Microglial reactivity to beta-amyloid is modulated by astrocytes and proinflammatory factors,” Brain Research, vol. 1025, no. 1-2, pp. 186–193, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Li, J. Lu, S. S. Tay, S. M. Moochhala, and B. P. He, “The function of microglia, either neuroprotection or neurotoxicity, is determined by the equilibrium among factors released from activated microglia in vitro,” Brain Research, vol. 1159, pp. 8–17, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Nakajima, Y. Tohyama, S. Maeda, S. Kohsaka, and T. Kurihara, “Neuronal regulation by which microglia enhance the production of neurotrophic factors for GABAergic, catecholaminergic, and cholinergic neurons,” Neurochemistry International, vol. 50, no. 6, pp. 807–820, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. J. V. Welser-Alves and R. Milner, “Microglia are the major source of TNF-α and TGF-β1 in postnatal glial cultures; regulation by cytokines, lipopolysaccharide, and vitronectin,” Neurochemistry International, vol. 63, no. 1, pp. 47–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. R. von Bernhardi, F. Cornejo, G. E. Parada, and J. Eugenin, “Role of TGFβ signaling in the pathogenesis of Alzheimer’s disease,” Frontiers in Cellular Neuroscience, vol. 9, p. 426, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Franco and D. Fernandez-Suarez, “Alternatively activated microglia and macrophages in the central nervous system,” Progress in Neurobiology, vol. 131, pp. 65–86, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. J. D. Cherry, J. A. Olschowka, and M. K. O'Banion, “Are “resting” microglia more “m2”?” Frontiers in Immunology, vol. 5, p. 594, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Tang and W. Le, “Differential roles of M1 and M2 microglia in neurodegenerative diseases,” Molecular Neurobiology, vol. 53, no. 2, pp. 1181–1194, 2016. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Herrera-Molina and R. von Bernhardi, “Transforming growth factor-beta 1 produced by hippocampal cells modulates microglial reactivity in culture,” Neurobiology of Disease, vol. 19, no. 1-2, pp. 229–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Ramirez, R. Toro, H. Dobeli, and R. von Bernhardi, “Protection of rat primary hippocampal cultures from A beta cytotoxicity by pro-inflammatory molecules is mediated by astrocytes,” Neurobiology of Disease, vol. 19, no. 1-2, pp. 243–254, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Wyss-Coray, C. Lin, F. Yan et al., “TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice,” Nature Medicine, vol. 7, no. 5, pp. 612–618, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. R. Derynck and Y. E. Zhang, “Smad-dependent and Smad-independent pathways in TGF-beta family signalling,” Nature, vol. 425, no. 6958, pp. 577–584, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Weiss and L. Attisano, “The TGFbeta superfamily signaling pathway,” Wiley Interdisciplinary Reviews: Developmental Biology, vol. 2, no. 1, pp. 47–63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Saud, R. Herrera-Molina, and R. Von Bernhardi, “Pro- and anti-inflammatory cytokines regulate the ERK pathway: implication of the timing for the activation of microglial cells,” Neurotoxicity Research, vol. 8, no. 3-4, pp. 277–287, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Horio, M. Kohno, Y. Fujita et al., “Levels of D-serine in the brain and peripheral organs of serine racemase (Srr) knock-out mice,” Neurochemistry International, vol. 59, no. 6, pp. 853–859, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. E. J. Perez, S. A. Tapanes, Z. B. Loris et al., “Enhanced astrocytic d-serine underlies synaptic damage after traumatic brain injury,” The Journal of Clinical Investigation, vol. 127, no. 8, pp. 3114–3125, 2017. View at Publisher · View at Google Scholar · View at Scopus
  72. J. M. Zhang and J. An, “Cytokines, inflammation, and pain,” International Anesthesiology Clinics, vol. 45, no. 2, pp. 27–37, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. S. W. Barger and A. S. Basile, “Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function,” Journal of Neurochemistry, vol. 76, no. 3, pp. 846–854, 2001. View at Google Scholar
  74. A. Young, “Ageing and physiological functions,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 352, no. 1363, pp. 1837–1843, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. R. G. Smith, L. Betancourt, and Y. Sun, “Molecular endocrinology and physiology of the aging central nervous system,” Endocrine Reviews, vol. 26, no. 2, pp. 203–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. R. L. Yung and A. Julius, “Epigenetics, aging, and autoimmunity,” Autoimmunity, vol. 41, no. 4, pp. 329–335, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. L. A. Lipsitz and A. L. Goldberger, “Loss of “complexity” and aging. Potential applications of fractals and chaos theory to senescence,” JAMA, vol. 267, no. 13, pp. 1806–1809, 1992. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Larbi, C. Franceschi, D. Mazzatti, R. Solana, A. Wikby, and G. Pawelec, “Aging of the immune system as a prognostic factor for human longevity,” Physiology, vol. 23, no. 2, pp. 64–74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. C. K. Lee, R. Weindruch, and T. A. Prolla, “Gene-expression profile of the ageing brain in mice,” Nature Genetics, vol. 25, no. 3, pp. 294–297, 2000. View at Publisher · View at Google Scholar · View at Scopus
  80. J. P. de Magalhaes, J. Curado, and G. M. Church, “Meta-analysis of age-related gene expression profiles identifies common signatures of aging,” Bioinformatics, vol. 25, no. 7, pp. 875–881, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. M. L. Block, L. Zecca, and J. S. Hong, “Microglia-mediated neurotoxicity: uncovering the molecular mechanisms,” Nature Reviews Neuroscience, vol. 8, no. 1, pp. 57–69, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. R. von Bernhardi, “Glial cell dysregulation: a new perspective on Alzheimer disease,” Neurotoxicity Research, vol. 12, no. 4, pp. 215–232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. H. M. Gao and J. S. Hong, “Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression,” Trends in Immunology, vol. 29, no. 8, pp. 357–365, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Akiyama, S. Barger, S. Barnum et al., “Inflammation and Alzheimer’s disease,” Neurobiology of Aging, vol. 21, no. 3, pp. 383–421, 2000. View at Publisher · View at Google Scholar · View at Scopus
  85. M. T. Heneka and M. K. O'Banion, “Inflammatory processes in Alzheimer’s disease,” Journal of Neuroimmunology, vol. 184, no. 1-2, pp. 69–91, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. E. C. Hirsch and S. Hunot, “Neuroinflammation in Parkinson’s disease: a target for neuroprotection?” Lancet Neurology, vol. 8, no. 4, pp. 382–397, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. M. D. Nguyen, J. P. Julien, and S. Rivest, “Innate immunity: the missing link in neuroprotection and neurodegeneration?” Nature Reviews. Neuroscience, vol. 3, no. 3, pp. 216–227, 2002. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Bjorkqvist, E. J. Wild, and S. J. Tabrizi, “Harnessing immune alterations in neurodegenerative diseases,” Neuron, vol. 64, no. 1, pp. 21–24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Sanjabi, L. A. Zenewicz, M. Kamanaka, and R. A. Flavell, “Anti-inflammatory and pro-inflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity,” Current Opinion in Pharmacology, vol. 9, no. 4, pp. 447–453, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. Zhu, C. Culmsee, S. Klumpp, and J. Krieglstein, “Neuroprotection by transforming growth factor-β1 involves activation of nuclear factor-κB through phosphatidylinositol-3-OH kinase/Akt and mitogen-activated protein kinase-extracellular-signal regulated kinase1,2 signaling pathways,” Neuroscience, vol. 123, no. 4, pp. 897–906, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Rota, G. Bellone, P. Rocca, B. Bergamasco, G. Emanuelli, and P. Ferrero, “Increased intrathecal TGF-β1, but not IL-12, IFN-γ and IL-10 levels in Alzheimer’s disease patients,” Neurological Sciences, vol. 27, no. 1, pp. 33–39, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Motta, R. Imbesi, M. Di Rosa, F. Stivala, and L. Malaguarnera, “Altered plasma cytokine levels in Alzheimer’s disease: correlation with the disease progression,” Immunology Letters, vol. 114, no. 1, pp. 46–51, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. G. Ramirez, S. Rey, and R. von Bernhardi, “Proinflammatory stimuli are needed for induction of microglial cell-mediated AβPP244-C and Aβ-neurotoxicity in hippocampal cultures,” Journal of Alzheimer's Disease, vol. 15, no. 1, pp. 45–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. R. C. Ewald and H. T. Cline, “NMDA receptors and brain development,” in Biology of the NMDA Receptor, A. M. Dongen, Ed., Taylor & Francis, Boca Raton, FL, USA, 2009. View at Google Scholar
  95. S. A. Fuchs, L. Dorland, M. G. de Sain-van der Velden et al., “D-serine in the developing human central nervous system,” Annals of Neurology, vol. 60, no. 4, pp. 476–480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. J. Jaeken, M. Detheux, L. Van Maldergem et al., “3-Phosphoglycerate dehydrogenase deficiency and 3-phosphoserine phosphatase deficiency: inborn errors of serine biosynthesis,” Journal of Inherited Metabolic Disease, vol. 19, no. 2, pp. 223–226, 1996. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Grassi and V. E. Pettorossi, “Synaptic plasticity in the medial vestibular nuclei: role of glutamate receptors and retrograde messengers in rat brainstem slices,” Progress in Neurobiology, vol. 64, no. 6, pp. 527–553, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. D. Yamazaki, J. Horiuchi, K. Ueno et al., “Glial dysfunction causes age-related memory impairment in Drosophila,” Neuron, vol. 84, no. 4, pp. 753–763, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. B. Potier, F. R. Turpin, P. M. Sinet et al., “Contribution of the d-serine-dependent pathway to the cellular mechanisms underlying cognitive aging,” Frontiers in Aging Neuroscience, vol. 2, p. 1, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Alliot, S. Boghossian, D. Jourdan et al., “The LOU/c/jall rat as an animal model of healthy aging?” The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, vol. 57, no. 8, pp. B312–B320, 2002. View at Publisher · View at Google Scholar · View at Scopus
  101. K. Eckles-Smith, D. Clayton, P. Bickford, and M. D. Browning, “Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression,” Molecular Brain Research, vol. 78, no. 1-2, pp. 154–162, 2000. View at Publisher · View at Google Scholar · View at Scopus
  102. N. Hori, I. Hirotsu, P. J. Davis, and D. O. Carpenter, “Long-term potentiation is lost in aged rats but preserved by calorie restriction,” Neuroreport, vol. 3, no. 12, pp. 1085–1088, 1992. View at Publisher · View at Google Scholar · View at Scopus
  103. C. Veyrat-Durebex and J. Alliot, “Changes in pattern of macronutrient intake during aging in male and female rats,” Physiology & Behavior, vol. 62, no. 6, pp. 1273–1278, 1997. View at Publisher · View at Google Scholar · View at Scopus
  104. R. Gredilla, M. Lopez-Torres, and G. Barja, “Effect of time of restriction on the decrease in mitochondrial H2O2 production and oxidative DNA damage in the heart of food-restricted rats,” Microscopy Research and Technique, vol. 59, no. 4, pp. 273–277, 2002. View at Publisher · View at Google Scholar · View at Scopus
  105. M. E. Walsh, Y. Shi, and H. Van Remmen, “The effects of dietary restriction on oxidative stress in rodents,” Free Radical Biology & Medicine, vol. 66, pp. 88–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. I. K. H. Hadem, T. Majaw, B. Kharbuli, and R. Sharma, “Beneficial effects of dietary restriction in aging brain,” Journal of Chemical Neuroanatomy, 2017. View at Publisher · View at Google Scholar · View at Scopus
  107. V. Jagannath, Z. Marinova, C. M. Monoranu, S. Walitza, and E. Grunblatt, “Expression of D-amino acid oxidase (DAO/DAAO) and D-amino acid oxidase activator (DAOA/G72) during development and aging in the human post-mortem brain,” Frontiers in Neuroanatomy, vol. 11, p. 31, 2017. View at Publisher · View at Google Scholar · View at Scopus
  108. C. H. Lin, H. T. Yang, C. C. Chiu, and H. Y. Lane, “Blood levels of D-amino acid oxidase vs. D-amino acids in reflecting cognitive aging,” Scientific Reports, vol. 7, no. 1, p. 14849, 2017. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Li, Y. Uno, U. Rudolph et al., “Astrocytes in primary cultures express serine racemase, synthesize d-serine and acquire A1 reactive astrocyte features,” Biochemical Pharmacology, vol. 151, pp. 245–251, 2018. View at Publisher · View at Google Scholar · View at Scopus
  110. A. Lourbopoulos, A. Erturk, and F. Hellal, “Microglia in action: how aging and injury can change the brain’s guardians,” Frontiers in Cellular Neuroscience, vol. 9, p. 54, 2015. View at Publisher · View at Google Scholar · View at Scopus
  111. L. Klapal, B. A. Igelhorst, and I. D. Dietzel-Meyer, “Changes in neuronal excitability by activated microglia: differential Na+ current upregulation in pyramid-shaped and bipolar neurons by TNF-α and IL-18,” Frontiers in Neurology, vol. 7, p. 44, 2016. View at Publisher · View at Google Scholar · View at Scopus
  112. S. A. Liddelow, K. A. Guttenplan, L. E. Clarke et al., “Neurotoxic reactive astrocytes are induced by activated microglia,” Nature, vol. 541, no. 7638, pp. 481–487, 2017. View at Publisher · View at Google Scholar · View at Scopus
  113. B. Zhao, Q. Wang, J. Du, S. Luo, J. Xia, and Y. G. Chen, “PICK1 promotes caveolin-dependent degradation of TGF-β type I receptor,” Cell Research, vol. 22, no. 10, pp. 1467–1478, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Fujii, K. Maeda, T. Hikida et al., “Serine racemase binds to PICK1: potential relevance to schizophrenia,” Molecular Psychiatry, vol. 11, no. 2, pp. 150–157, 2006. View at Publisher · View at Google Scholar · View at Scopus
  115. C. Vargas-Lopes, C. Madeira, S. A. Kahn et al., “Protein kinase C activity regulates D-serine availability in the brain,” Journal of Neurochemistry, vol. 116, no. 2, pp. 281–290, 2011. View at Publisher · View at Google Scholar · View at Scopus
  116. Y. N. Wang, L. Zhou, Y. H. Li et al., “Protein interacting with C-kinase 1 deficiency impairs glutathione synthesis and increases oxidative stress via reduction of surface excitatory amino acid carrier 1,” The Journal of Neuroscience, vol. 35, no. 16, pp. 6429–6443, 2015. View at Publisher · View at Google Scholar · View at Scopus
  117. J. Zhu, Z. Wang, N. Zhang et al., “Protein interacting C-kinase 1 modulates surface expression of P2Y6 purinoreceptor, actin polymerization and phagocytosis in microglia,” Neurochemical Research, vol. 41, no. 4, pp. 795–803, 2016. View at Publisher · View at Google Scholar · View at Scopus
  118. M. C. Focant and E. Hermans, “Protein interacting with C kinase and neurological disorders,” Synapse, vol. 67, no. 8, pp. 532–540, 2013. View at Publisher · View at Google Scholar · View at Scopus
  119. Y. Yang, W. Ge, Y. Chen et al., “Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 15194–15199, 2003. View at Publisher · View at Google Scholar · View at Scopus
  120. S. A. Fuchs, M. G. de Sain-van der Velden, M. M. de Barse et al., “Two mass-spectrometric techniques for quantifying serine enantiomers and glycine in cerebrospinal fluid: potential confounders and age-dependent ranges,” Clinical Chemistry, vol. 54, no. 9, pp. 1443–1450, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. G. Bain, W. J. Ray, M. Yao, and D. I. Gottlieb, “From embryonal carcinoma cells to neurons: the P 19 pathway,” BioEssays, vol. 16, no. 5, pp. 343–348, 1994. View at Publisher · View at Google Scholar · View at Scopus
  122. S. A. Fuchs, M. W. Roeleveld, L. W. Klomp, R. Berger, and T. J. de Koning, “D-serine influences synaptogenesis in a p19 cell model,” in JIMD Reports - Case and Research Reports, 2012/3, SSIEM, Ed., vol. 6 of JIMD Reports, pp. 47–53, Springer, Berlin, Heidelberg, 2012. View at Publisher · View at Google Scholar
  123. P. M. Kim, H. Aizawa, P. S. Kim et al., “Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 6, pp. 2105–2110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  124. H. Zhang, L. Song, Y. Chang et al., “Potential deficit from decreased cerebellar granule cell migration in serine racemase-deficient mice is reversed by increased expression of GluN2B and elevated levels of NMDAR agonists,” Molecular and Cellular Neurosciences, vol. 85, pp. 119–126, 2017. View at Publisher · View at Google Scholar · View at Scopus
  125. H. Han, Y. Peng, and Z. Dong, “D-serine rescues the deficits of hippocampal long-term potentiation and learning and memory induced by sodium fluoroacetate,” Pharmacology, Biochemistry, and Behavior, vol. 133, pp. 51–56, 2015. View at Publisher · View at Google Scholar · View at Scopus
  126. M. Kollen, A. Stephan, A. Faivre-Bauman et al., “Preserved memory capacities in aged Lou/C/Jall rats,” Neurobiology of Aging, vol. 31, no. 1, pp. 129–142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. A. Miyamoto, H. Wake, A. W. Ishikawa et al., “Microglia contact induces synapse formation in developing somatosensory cortex,” Nature Communications, vol. 7, article 12540, 2016. View at Publisher · View at Google Scholar · View at Scopus
  128. D. P. Schafer, E. K. Lehrman, A. G. Kautzman et al., “Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner,” Neuron, vol. 74, no. 4, pp. 691–705, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. C. N. Parkhurst, G. Yang, I. Ninan et al., “Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor,” Cell, vol. 155, no. 7, pp. 1596–1609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  130. D. W. Choi, J. Y. Koh, and S. Peters, “Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists,” The Journal of Neuroscience, vol. 8, no. 1, pp. 185–196, 1988. View at Publisher · View at Google Scholar
  131. G. E. Hardingham and H. Bading, “Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders,” Nature Reviews Neuroscience, vol. 11, no. 10, pp. 682–696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. M. P. Parsons and L. A. Raymond, “Extrasynaptic NMDA receptor involvement in central nervous system disorders,” Neuron, vol. 82, no. 2, pp. 279–293, 2014. View at Publisher · View at Google Scholar · View at Scopus
  133. T. Papouin, L. Ladepeche, J. Ruel et al., “Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists,” Cell, vol. 150, no. 3, pp. 633–646, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. X. Zhou, D. Hollern, J. Liao, E. Andrechek, and H. Wang, “NMDA receptor-mediated excitotoxicity depends on the coactivation of synaptic and extrasynaptic receptors,” Cell Death & Disease, vol. 4, no. 3, p. e560, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. E. H. Lo, A. R. Pierce, K. Matsumoto, T. Kano, C. J. Evans, and R. Newcomb, “Alterations in K+ evoked profiles of neurotransmitter and neuromodulator amino acids after focal ischemia-reperfusion,” Neuroscience, vol. 83, no. 2, pp. 449–458, 1998. View at Publisher · View at Google Scholar · View at Scopus
  136. H. Katsuki, M. Nonaka, H. Shirakawa, T. Kume, and A. Akaike, “Endogenous D-serine is involved in induction of neuronal death by N-methyl-D-aspartate and simulated ischemia in rat cerebrocortical slices,” The Journal of Pharmacology and Experimental Therapeutics, vol. 311, no. 2, pp. 836–844, 2004. View at Publisher · View at Google Scholar · View at Scopus
  137. H. S. Choi, D. H. Roh, S. Y. Yoon et al., “Differential involvement of ipsilateral and contralateral spinal cord astrocyte D-serine in carrageenan-induced mirror-image pain: role of sigma 1 receptors and astrocyte gap junctions,” British Journal of Pharmacology, vol. 175, no. 3, pp. 558–572, 2018. View at Publisher · View at Google Scholar · View at Scopus
  138. P. Moore, A. El-sherbeny, P. Roon, P. V. Schoenlein, V. Ganapathy, and S. B. Smith, “Apoptotic cell death in the mouse retinal ganglion cell layer is induced in vivo by the excitatory amino acid homocysteine,” Experimental Eye Research, vol. 73, no. 1, pp. 45–57, 2001. View at Publisher · View at Google Scholar · View at Scopus
  139. H. Jiang, J. Fang, B. Wu et al., “Overexpression of serine racemase in retina and overproduction of D-serine in eyes of streptozotocin-induced diabetic retinopathy,” Journal of Neuroinflammation, vol. 8, no. 1, p. 119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  140. H. Ozaki, R. Inoue, T. Matsushima, M. Sasahara, A. Hayashi, and H. Mori, “Serine racemase deletion attenuates neurodegeneration and microvascular damage in diabetic retinopathy,” PLoS One, vol. 13, no. 1, article e0190864, 2018. View at Publisher · View at Google Scholar · View at Scopus
  141. C. Madeira, M. V. Lourenco, C. Vargas-Lopes et al., “D-serine levels in Alzheimer’s disease: implications for novel biomarker development,” Translational Psychiatry, vol. 5, no. 5, article e561, 2015. View at Publisher · View at Google Scholar · View at Scopus
  142. Y. Nagata, M. Borghi, G. H. Fisher, and A. D'Aniello, “Free D-serine concentration in normal and Alzheimer human brain,” Brain Research Bulletin, vol. 38, no. 2, pp. 181–183, 1995. View at Publisher · View at Google Scholar · View at Scopus
  143. E. A. Biemans, N. M. Verhoeven-Duif, J. Gerrits, J. A. Claassen, H. B. Kuiperij, and M. M. Verbeek, “CSF d-serine concentrations are similar in Alzheimer’s disease, other dementias, and elderly controls,” Neurobiology of Aging, vol. 42, pp. 213–216, 2016. View at Publisher · View at Google Scholar · View at Scopus
  144. K. Hashimoto, T. Fukushima, E. Shimizu et al., “Possible role of D-serine in the pathophysiology of Alzheimer’s disease,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, vol. 28, no. 2, pp. 385–388, 2004. View at Publisher · View at Google Scholar · View at Scopus