Oleic Acid and Cholinergic dysfunction in Down Syndrome Models of the Central Nervous System

  1. Velasco, Ana 1
  2. Maruan Hijazi 1
  1. 1 Departamento de Bioquímica y Biología Molecular, Instituto de Neurociencias de Castilla y León
Journal:
Journal of Neurology and Neuromedicine

ISSN: 2572-942X

Year of publication: 2016

Volume: 1

Issue: 3

Pages: 1-5

Type: Article

DOI: 10.29245/2572.942X/2016/3.1029 GOOGLE SCHOLAR

More publications in: Journal of Neurology and Neuromedicine

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Abstract

Down syndrome (DS): or trisomy 21: is the most common autosomal aneuploidy and the leading genetic cause of intellectual disability. It is widely established that mental retardation is primarily a consequence of brain functioning and developmental abnormalities in neurogenesis. Some changes in the physical structure of the dendrites are a major cause of impaired synaptic plasticity of DS. The overexpression of the dual specificyty tyrsone phosphorylation- regulated kinase 1A (DYRK1A): located on chromosome 21: is involved in cellular plasticity and responsible for central nervous system disturbance in DS. Oleic acid is a neurotrophic factor that promotes neuronal differentiation and increases the levels of choline acetyltransferase (ChAT). Furthermore: it has recently been shown that it induces migration and formation of new synapses in euploid cells. However: remarkably oleic acid fails to reproduce the same effects in trisomic cells. Here we review the hypothesis that oleic acid-dependent synaptic plasticity may be dependent on the lipid environment. Thus: differences in membrane composition may be essential to understand why oleic acid promotes higher cell plasticity in euploid than in trisomic cells.

Bibliographic References

  • 1. Rachidi M, Lopes C. Molecular and cellular mechanisms elucidating neurocognitive basis of functional impairments associated with intellectual disability in Down syndrome. Am J Intellect Dev Disabil. 2010; 115(2): 83-112.
  • 2. Dierssen M. Down syndrome: the brain in trisomic mode. Nat Rev Neurosci. 2012; 13(12): 844-58.
  • 3. Golden JA, Hyman BT. Development of the superior temporal neocortex is anomalous in trisomy 21. J Neuropathol Exp Neurol. 1994; 53(5): 513-20.
  • 4. Becker L, Mito T, Takashima S, Onodera K. Growth and development of the brain in Down syndrome. Prog Clin Biol Res. 1991; 373: 133-52.
  • 5. Rueda N, Flórez J, Martínez-Cué C. Mouse models of Down syndrome as a tool to unravel the causes of mental disabilities. Neural Plast. 2012; 2012: 584071.
  • 6. Tabernero A, Velasco A, Granda B, Lavado EM, Medina JM. Transcytosis of albumin in astrocytes activates the sterol regulatory element- binding protein-1, which promotes the synthesis of the neurotrophic factor oleic acid. J Biol Chem. 2002; 277(6): 4240-6.
  • 7. Alberts B. Molecular Biology of the Cell. 2008.
  • 8. Tabernero A, Lavado EM, Granda B, Velasco A, Medina JM. Neuronal differentiation is triggered by oleic acid synthesized and released by astrocytes. J Neurochem. 2001; 79(3): 606-16.
  • 9. Polo-Hernández E, De Castro F, García-García AG, Tabernero A, Medina JM. Oleic acid synthesized in the periventricular zone promotes axonogenesis in the striatum during brain development. J Neurochem. 2010; 114(6): 1756-66.
  • 10. García-García AG, Polo-Hernández E, Tabernero A, Medina JM. Alpha- fetoprotein (AFP) modulates the effect of serum albumin on brain development by restraining the neurotrophic effect of oleic acid. Brain Res. 2015; 1624: 45-58.
  • 11. Haydar TF, Blue ME, Molliver ME, Krueger BK, Yarowsky PJ. Consequences of trisomy 16 for mouse brain development: corticogenesis in a model of Down syndrome. J Neurosci. 1996; 16(19): 6175-82.
  • 12. Laffaire J, Rivals I, Dauphinot L, Pasteau F, Wehrle R, Larrat B, et al. Gene expression signature of cerebellar hypoplasia in a mouse model of Down syndrome during postnatal development. BMC Genomics. 2009; 10: 138.
  • 13. Roper RJ, Baxter LL, Saran NG, Klinedinst DK, Beachy PA, Reeves RH. Defective cerebellar response to mitogenic Hedgehog signaling in Down [corrected] syndrome mice. Proc Natl Acad Sci U S A. 2006; 103(5): 1452-6.
  • 14. Altafaj X, Dierssen M, Baamonde C, Martí E, Visa J, Guimerà J, et al. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down’s syndrome. Hum Mol Genet. 2001; 10(18): 1915-23.
  • 15. Arqué G, Fotaki V, Fernández D, Martínez de Lagrán M, Arbonés ML, Dierssen M. Impaired spatial learning strategies and novel object recognition in mice haploinsufficient for the dual specificity tyrosine- regulated kinase-1A (Dyrk1A). PLoS One. 2008; 3(7): e2575.
  • 16. Cheon MS, Kim SH, Fountoulakis M, Lubec G. Heart type fatty acid binding protein (H-FABP) is decreased in brains of patients with Down syndrome and Alzheimer’s disease. J Neural Transm Suppl. 2003(67): 225-34.
  • 17. Tejedor FJ, Hammerle B. MNB/DYRK1A as a multiple regulator of neuronal development. FEBS J. 2011; 278(2): 223-35.
  • 18. Saud K, Arriagada C, Cárdenas AM, Shimahara T, Allen DD, Caviedes R, et al. Neuronal dysfunction in Down syndrome: contribution of neuronal models in cell culture. J Physiol Paris. 2006; 99(2-3): 201-10.
  • 19. Opazo P, Saud K, de Saint Pierre M, Cárdenas AM, Allen DD, Segura- Aguilar J, et al. Knockdown of amyloid precursor protein normalizes cholinergic function in a cell line derived from the cerebral cortex of a trisomy 16 mouse: An animal model of down syndrome. J Neurosci Res. 2006; 84(6): 1303-10.
  • 20. Hijazi M, Fillat C, Medina JM, Velasco A. Overexpression of DYRK1A inhibits choline acetyltransferase induction by oleic acid in cellular models of Down syndrome. Exp Neurol. 2013; 239: 229-34.
  • 21. Bento-Abreu A, Tabernero A, Medina JM. Peroxisome proliferator- activated receptor-alpha is required for the neurotrophic effect of oleic acid in neurons. J Neurochem. 2007; 103(3): 871-81.
  • 22. Rodríguez-Rodríguez RA, Tabernero A, Velasco A, Lavado EM, Medina JM. The neurotrophic effect of oleic acid includes dendritic differentiation and the expression of the neuronal basic helix-loop- helix transcription factor NeuroD2. J Neurochem. 2004; 88(5): 1041- 51.
  • 23. Allen DD, Martín J, Arriagada C, Cárdenas AM, Rapoport SI, Caviedes R, et al. Impaired cholinergic function in cell lines derived from the cerebral cortex of normal and trisomy 16 mice. Eur J Neurosci. 2000; 12(9): 3259-64.
  • 24. Ozand PT, Hawkins RL, Collins RM Jr, Reed WD, Baab PJ, Oster-Granite ML. Neurochemical changes in murine trisomy 16: delay in cholinergic and catecholaminergic systems. J Neurochem. 1984; 43(2): 401-8.
  • 25. Sweeney JE, Höhmann CF, Oster-Granite ML, Coyle JT. Neurogenesis of the basal forebrain in euploid and trisomy 16 mice: an animal model for developmental disorders in Down syndrome. Neuroscience. 1989; 31(2): 413-25.
  • 26. Fiedler JL, Epstein CJ, Rapoport SI, Caviedes R, Caviedes P. Regional alteration of cholinergic function in central neurons of trisomy 16 mouse fetuses, an animal model of human trisomy 21 (Down syndrome). Brain Res. 1994; 658(1-2): 27-32.
  • 27. Yates CM, Simpson J, Gordon A, Maloney AF, Allison Y, Ritchie IM, et al. Catecholamines and cholinergic enzymes in pre-senile and senile Alzheimer-type dementia and Down’s syndrome. Brain Res. 1983; 280(1): 119-26.
  • 28. Kish S, Karlinsky H, Becker L, Gilbert J, Rebbetoy M, Chang LJ, et al. Down’s syndrome individuals begin life with normal levels of brain cholinergic markers. J Neurochem. 1989; 52(4): 1183-7.
  • 29. Lubec B, Yoo BC, Dierssen M, Balic N, Lubec G. Down syndrome patients start early prenatal life with normal cholinergic, monoaminergic and serotoninergic innervation. J Neural Transm Suppl. 2001; 61: 303-10.
  • 30. Massarelli R, Ferret B, Sorrentino G, Hattori H, Kanfer JN. Choline acetyltransferase-like activity bound to neuronal plasma membranes. Neurochem Res. 1988; 13(12): 1193-8.
  • 31. Hattori H, Kanfer JN, Massarelli R. Stimulation of phospholipase D activity and indication of acetylcholine synthesis by oleate in rat brain synaptosomal preparations. Neurochem Res. 1987; 12(8): 687-92.
  • 32. Machová E, Málková B, Lisá V, Nováková J, Dolezal V. The increase of choline acetyltransferase activity by docosahexaenoic acid in NG108- 15 cells grown in serum-free medium is independent of its effect on cell growth. Neurochem Res. 2006; 31(10): 1239-46.
  • 33. Murphy EJ, Schapiro MB, Rapoport SI, Shetty HU. Phospholipid composition and levels are altered in Down syndrome brain. Brain Res. 2000; 867(1-2): 9-18.
  • 34. Shah SN. Fatty acid composition of lipids of human brain myelin and synaptosomes: changes in phenylketonuria and Down’s syndrome. Int J Biochem. 1979; 10(6): 477-82.
  • 35. Elul R, Hanley J, Simmons JQ 3 rd . Non-Gaussian behavior of the EEG in Down’s syndrome suggests decreased neuronal connections. Acta Neurol Scand. 1975; 51(1): p. 21-28.
  • 36. Hijazi M, Medina JM, Velasco A. Restrained Phosphatidylcholine Synthesis in a Cellular Model of Down’s Syndrome is Associated with the Overexpression of Dyrk1A. Mol Neurobiol. 2016.
  • 37. Medina JM, Tabernero A. Astrocyte-synthesized oleic acid behaves as a neurotrophic factor for neurons. J Physiol Paris. 2002; 96(3-4): 265- 71.
  • 38. Lopez S, Bermudez B, Montserrat-de la Paz S, Jaramillo S, Varela LM, Ortega-Gomez A, et al. Membrane composition and dynamics: A target of bioactive virgin olive oil constituents. Biochim Biophys Acta. 2014; 1838(6): 1638-56.
  • 39. Vance DE. Physiological roles of phosphatidylethanolamine N-methyltransferase. Biochim Biophys Acta. 2013; 1831(3): 626-32.
  • 40. Planque C, Dairou J, Noll C, Bui LC, Ripoll C, Guedj F, et al. Mice deficient in cystathionine beta synthase display increased Dyrk1A and SAHH activities in brain. J Mol Neurosci. 2013; 50(1): 1-6.