Article thumbnail

Sensory Experience Differentially Modulates the mRNA Expression of the Polysialyltransferases ST8SiaII and ST8SiaIV in Postnatal Mouse Visual Cortex

By Marie-Claude Bélanger and Graziella Di Cristo

Abstract

Polysialic acid (PSA) is a unique carbohydrate composed of a linear homopolymer of α-2,8 linked sialic acid, and is mainly attached to the fifth immunoglobulin-like domain of the neural cell adhesion molecule (NCAM) in vertebrate neural system. In the brain, PSA is exclusively synthesized by the two polysialyltransferases ST8SiaII (also known as STX) and ST8SiaIV (also known as PST). By modulating adhesive property of NCAM, PSA plays a critical role in several neural development processes such as cell migration, neurite outgrowth, axon pathfinding, synaptogenesis and activity-dependent plasticity. The expression of PSA is temporally and spatially regulated during neural development and a tight regulation of PSA expression is essential to its biological function. In mouse visual cortex, PSA is downregulated following eye opening and its decrease allows the maturation of GABAergic synapses and the opening of the critical period for ocular dominance plasticity. Relatively little is known about how PSA levels are regulated by sensory experience and neuronal activity. Here, we demonstrate that while both ST8SiaII and ST8SiaIV mRNA levels decrease around the time of eye opening in mouse visual cortex, only ST8SiaII mRNA level reduction is regulated by sensory experience. Using an organotypic culture system from mouse visual cortex, we further show that ST8SiaII gene expression is regulated by spiking activity and NMDA-mediated excitation. Further, we show that both ST8SiaII and ST8SiaIV mRNA levels are positively regulated by PKC-mediated signaling. Therefore, sensory experience-dependent ST8SiaII gene expression regulates PSA levels in postnatal visual cortex, thus acting as molecular link between visual activity and PSA expression

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3177851
Provided by: PubMed Central

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.

Suggested articles

Citations

  1. (2001). A
  2. (2006). A brain-specific microRNA regulates dendritic spine development.
  3. (2010). A conserved switch in sensory processing prepares developing neocortex for vision.
  4. (2009). Activation of CaMKII in single dendritic spines during long-term potentiation.
  5. (2005). Activity dependence of cortical axon branch formation: a morphological and electrophysiological study using organotypic slice cultures.
  6. (2000). Activity-dependent development of spontaneous bioelectric activity in organotypic cultures of rat occipital cortex.
  7. (1994). Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells.
  8. (2007). Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity.
  9. (2006). Association between polymorphisms in the promoter region of the sialyltransferase 8B (SIAT8B) gene and schizophrenia.
  10. (2007). Blasco-Iba ´n ˜ez JM, Go ´mez-Climent MA, Castillo-Go ´mez
  11. (1999). Cell surface expression of polysialic acid on NCAM is a prerequisite for activitydependent morphological neuronal and glial plasticity.
  12. (2008). Communication between the synapse and the nucleus in neuronal development, plasticity, and disease.
  13. (1988). Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and ‘‘waiting periods’’.
  14. (2005). Critical period plasticity in local cortical circuits.
  15. (1982). Differences in the carbohydrate structures of neural cell-adhesion molecules from adult and embryonic chicken brains.
  16. (2005). Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion.
  17. (1993). Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system.
  18. (2008). Dopamine acting through D2 receptors modulates the expression of PSA-NCAM, a molecule related to neuronal structural plasticity, in the medial prefrontal cortex of adult rats. Exp Neurol.214:
  19. (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period.
  20. (1996). Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration.
  21. (2005). Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule.
  22. (1998). Heterogeneous expression of the polysialyltransferases ST8Sia II and ST8Sia IV during postnatal rat brain development.
  23. (2009). Imbalance of neural cell adhesion molecule and polysialyltransferase alleles causes defective brain connectivity.
  24. (2008). Impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid synthesis during postnatal mouse brain development.
  25. (2000). Inhibitory mechanism by polysialic acid for lamina-specific branch formation of thalamocortical axons.
  26. (2002). Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus.
  27. (2009). Mef2-mediated transcription of the miR379-410 cluster regulates activitydependent dendritogenesis by fine-tuning Pumilio2 protein levels.
  28. (2000). Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity.
  29. (2010). MicroRNA pathways in neural development and plasticity. Curr Opin Neurobiol.
  30. (1995). Molecular characterization of eukaryotic polysialyltransferase-1.
  31. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid.
  32. (2010). Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors.
  33. (1982). Neuronal discharge patterns in the occipital cortex of developing rats during active and quiet sleep.
  34. (2006). NFkappaB regulates spatial memory formation and synaptic plasticity through protein kinase A/CREB signaling.
  35. (2009). NMDA receptor activation increases free radical production through nitric oxide and NOX2.
  36. (1999). Patterns of spontaneous activity and morphology of interneuron types in organotypic cortex and thalamus-cortex cultures.
  37. (1993). Polymerase chain reaction cloning of a developmentally regulated member of the sialyltransferase gene family.
  38. (2008). Polysialic acid in the plasticity of the developing and adult vertebrate nervous system.
  39. (1992). Polysialic acid influences specific pathfinding by avian motoneurons.
  40. (2006). Polysialic acid limits choline acetyltransferase activity induced by brain-derived neurotrophic factor.
  41. (2004). Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses.
  42. (2004). Polysialylated neural cell adhesion molecule promotes remodeling and ormation of hippocampal synapses.
  43. (2007). Positive association between SIAT8B and schizophrenia in the Chinese Han population.
  44. (1997). Postnatal development of low [Mg 2+] oscillations in neocortex.
  45. (2001). Protein kinase C delta regulates neural cell adhesion molecule polysialylation state in the rat brain.
  46. (2006). PSA-NCAM in mammalian structural plasticity and neurogenesis.
  47. (1996). PSA-NCAM is required for activity-induced synaptic plasticity.
  48. (2001). PSANCAM modulates BDNF-dependent survival and differentiation of cortical neurons.
  49. (2001). Regulation of cell adhesion by polysialic acid. Effects on cadherin, immunoglobulin cell adhesion molecule and integrin function and independence from neural cell adhesion molecule binding or signaling activity.
  50. (1998). Regulation of neural cell adhesion molecule polysialylation: evidence for nontranscriptional control and sensitivity to an intracellular pool of calcium.
  51. (2001). Requirement of ERK activation for visual cortical plasticity.
  52. (2009). REST and CoREST modulate neuronal subtype specification, maturation and maintenance.
  53. (2004). Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior.
  54. (2008). SnapShot: Ca(2+)-dependent transcription in neurons.
  55. (2011). Structural and functional impairments of polysialic acid by a mutated polysialyltransferase found in schizophrenia.
  56. (2004). Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs.
  57. (2006). Use of polysialic acid in repair of the central nervous system.