Advertisement

Current Understanding of the Role of Neuronal Calcium Sensor 1 in Neurological Disorders

  • Julia Bandura
  • Zhong-Ping FengEmail author
Article
  • 45 Downloads

Abstract

Neuronal calcium sensor 1 (NCS-1) is a high-affinity calcium-binding protein and its ubiquitous expression in the nervous system implies a wide range of functions. To date, it has been implicated in regulation of calcium channels in both axonal growth cones and presynaptic terminals, pre- and postsynaptic plasticity mechanisms, learning and memory behaviors, dopaminergic signaling, and axonal regeneration. This review summarizes these functions and relates them to several diseases in which NCS-1 plays a role, such as schizophrenia and bipolar disorder, X-linked mental retardation and fragile X syndrome, and spinal cord injury. Many questions remain unanswered about the role of NCS-1 in these diseases, particularly as the genetic factors that control NCS-1 expression in both normal and diseased states are still poorly understood. The review further identifies the therapeutic potential of manipulating the interaction of NCS-1 with its many targets and suggests directions for future research on the role of NCS-1 in these disorders.

Keywords

NCS-1 Frequenin Calcium-binding proteins Schizophrenia Bipolar disorder X-linked mental retardation 

Notes

Acknowledgements

Molecular graphics and analyses were performed with UCSF Chimera, developed by the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco, with support from NIH P41-GM103311. JB is a recipient of an Ontatio Graduate Scholarship (OGS). This work is funded by a Canadian Institutes of Health Research (CIHR) Project Grant to Z.P.F. (CIHR-PJT-153155).

References

  1. 1.
    Braunewell KH, Gundelfinger ED (1999) Intracellular neuronal calcium sensor proteins: a family of EF hand calcium-binding proteins in search of a function. Cell Tissue Res 295:1–12.  https://doi.org/10.1007/s004410051207 CrossRefPubMedGoogle Scholar
  2. 2.
    Burgoyne RD, Weiss JL (2000) The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353:1–12.  https://doi.org/10.1042/bj3530001 CrossRefGoogle Scholar
  3. 3.
    Burgoyne RD, O’Callaghan DW, Hasdemir B et al (2004) Neuronal Ca2+-sensor proteins: multitalented regulators of neuronal function. Trends Neurosci 27:203–209.  https://doi.org/10.1016/j.tins.2004.01.010 CrossRefPubMedGoogle Scholar
  4. 4.
    De Castro E, Nef S, Fiumelli H et al (1995) Regulation of rhodopsin phosphorylation by a family of neuronal calcium sensors. Biochem Biophys Res Commun 216:133–140.  https://doi.org/10.1006/bbrc.1995.2601 CrossRefPubMedGoogle Scholar
  5. 5.
    Muralidhar D, Kunjachen Jobby M, Jeromin A, Roder J, Thomas F, Sharma Y (2004) Calcium and chlorpromazine binding to the EF-hand peptides of neuronal calcium sensor-1. Peptides 25:909–917.  https://doi.org/10.1016/j.peptides.2004.03.017 CrossRefPubMedGoogle Scholar
  6. 6.
    Aravind P, Chandra K, Reddy PP, Jeromin A, Chary KVR, Sharma Y (2008) Regulatory and structural EF-hand motifs of neuronal calcium sensor-1: Mg2+ modulates Ca2+ binding, Ca2+-induced conformational changes, and equilibrium unfolding transitions. J Mol Biol 376:1100–1115.  https://doi.org/10.1016/j.jmb.2007.12.033 CrossRefPubMedGoogle Scholar
  7. 7.
    Jeromin A, Muralidhar D, Parameswaran MN, Roder J, Fairwell T, Scarlata S, Dowal L, Mustafi SM et al (2004) N-terminal myristoylation regulates calcium-induced conformational changes in neuronal calcium sensor-1. J Biol Chem 279:27158–27167.  https://doi.org/10.1074/jbc.M312172200 CrossRefPubMedGoogle Scholar
  8. 8.
    Baksheeva V, Nazipova A, Zinchenko D, Serebryakova M, Senin I, Permyakov S, Philippov P, Li Y et al (2015) Ca2+-myristoyl switch in neuronal calcium sensor-1: a role of C-terminal segment. CNS Neurol Disord Drug Targets 14:437–451.  https://doi.org/10.2174/1871527314666150225143403 CrossRefPubMedGoogle Scholar
  9. 9.
    Kabbani N, Negyessy L, Lin R, Goldman-Rakic P, Levenson R (2002) Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor. J Neurosci 22:8476–8486.  https://doi.org/10.1523/JNEUROSCI.22-19-08476.2002 CrossRefPubMedGoogle Scholar
  10. 10.
    Pandalaneni S, Karuppiah V, Saleem M, Haynes LP, Burgoyne RD, Mayans O, Derrick JP, Lian LY (2015) Neuronal calcium sensor-1 binds the D2 dopamine receptor and G-protein-coupled receptor kinase 1 (GRK1) peptides using different modes of interactions. J Biol Chem 290:18744–18756.  https://doi.org/10.1074/jbc.M114.627059 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Pettersen E, Goddard T, Huang C et al (2004) UCSF chimera--a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612.  https://doi.org/10.1002/jcc.20084 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Nef S, Fiumelli H, De Castro E et al (1995) Identification of a neuronal calcium sensor (NCS-1) possible involved in the regulation of receptor phosphorylation. J Recept Signal Transduct Res 15:365–378.  https://doi.org/10.3109/10799899509045227 CrossRefPubMedGoogle Scholar
  13. 13.
    Martone ME, Edelmann VM, Ellisman MH, Nef P (1999) Cellular and subcellular distribution of the calcium-binding protein NCS-1 in the central nervous system of the rat. Cell Tissue Res 295:395–407.  https://doi.org/10.1007/s004410051246 CrossRefPubMedGoogle Scholar
  14. 14.
    Olafsson P, Soares HD, Herzog K-H et al (1997) The Ca2+ binding protein, frequenin is a nervous system-specific protein in mouse preferentially localized in neurites. Mol Brain Res 44:73–82.  https://doi.org/10.1016/S0896-6273(01)00434-2 CrossRefPubMedGoogle Scholar
  15. 15.
    Kawasaki T, Nishio T, Kurosawa H, Roder J, Jeromin A (2003) Spatiotemporal distribution of neuronal calcium sensor-1 in the developing rat spinal cord. J Comp Neurol 460:465–475.  https://doi.org/10.1002/cne.10649 CrossRefPubMedGoogle Scholar
  16. 16.
    Paterlini M, Revilla V, Grant AL, Wisden W (2000) Expression of the neuronal calcium sensor protein family in the rat brain. Neuroscience 99:205–216.  https://doi.org/10.1016/S0306-4522(00)00201-3 CrossRefPubMedGoogle Scholar
  17. 17.
    Averill S, Robson LG, Jeromin A, Priestley JV (2004) Neuronal calcium sensor-1 is expressed by dorsal root ganglion cells, is axonally transported to central and peripheral terminals, and is concentrated at nodes. Neuroscience 123:419–427.  https://doi.org/10.1016/j.neuroscience.2003.09.031 CrossRefPubMedGoogle Scholar
  18. 18.
    Reynolds AJ, Bartlett SE, Morgans C (2001) The distribution of neuronal calcium sensor-1 protein in the developing and adult rat retina. Neuroreport 12:725–728CrossRefGoogle Scholar
  19. 19.
  20. 20.
    Schaad NC, De Castro E, Nef S et al (1996) Direct modulation of calmodulin targets by the neuronal calcium sensor NCS-1. Proc Natl Acad Sci U S A 93:9253–9258.  https://doi.org/10.1073/pnas.93.17.9253 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Haynes LP, Fitzgerald DJ, Wareing B, O'Callaghan DW, Morgan A, Burgoyne RD (2006) Analysis of the interacting partners of the neuronal calcium-binding proteins L-CaBP1, hippocalcin, NCS-1 and neurocalcin δ. Proteomics 6:1822–1832.  https://doi.org/10.1002/pmic.200500489 CrossRefPubMedGoogle Scholar
  22. 22.
    Burgoyne RD (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8:182–193.  https://doi.org/10.1038/nrn2093 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Weiss JL, Hui H, Burgoyne RD (2010) Neuronal calcium sensor-1 regulation of calcium channels, secretion, and neuronal outgrowth. Cell Mol Neurobiol 30:1283–1292.  https://doi.org/10.1007/s10571-010-9588-7 CrossRefPubMedGoogle Scholar
  24. 24.
    Dason JS, Romero-Pozuelo J, Atwood HL, Ferrús A (2012) Multiple roles for frequenin/NCS-1 in synaptic function and development. Mol Neurobiol 45:388–402.  https://doi.org/10.1007/s12035-012-8250-4 CrossRefPubMedGoogle Scholar
  25. 25.
    Boeckel GR, Ehrlich BE (2018) NCS-1 is a regulator of calcium signaling in health and disease. Biochim Biophys Acta Mol Cell Res 1865:1660–1667.  https://doi.org/10.1016/j.bbamcr.2018.05.005 CrossRefGoogle Scholar
  26. 26.
    Südhof TC (2012) Calcium control of neurotransmitter release. Cold Spring Harb Perspect Biol 4:1–16.  https://doi.org/10.1101/cshperspect.a011353 CrossRefGoogle Scholar
  27. 27.
    Simms BA, Zamponi GW (2014) Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 82:24–45.  https://doi.org/10.1016/j.neuron.2014.03.016 CrossRefPubMedGoogle Scholar
  28. 28.
    Catterall WA, Few AP (2008) Calcium channel regulation and presynaptic plasticity. Neuron 59:882–901.  https://doi.org/10.1016/j.neuron.2008.09.005 CrossRefPubMedGoogle Scholar
  29. 29.
    Regehr WG (2012) Short-term presynaptic plasticity. Cold Spring Harb Perspect Biol 4:a005702.  https://doi.org/10.1101/cshperspect.a005702 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wang C-Y, Yang F, He X, Chow A, du J, Russell JT, Lu B (2001) Ca2+ binding protein frequenin mediates GDNF-induced potentiation of Ca2+ channels and transmitter release. Neuron 32:99–112.  https://doi.org/10.1016/S0896-6273(01)00434-2
  31. 31.
    Rousset M, Cens T, Gavarini S, Jeromin A, Charnet P (2003) Down-regulation of voltage-gated Ca2+ channels by neuronal calcium sensor-1 is β subunit-specific. J Biol Chem 278:7019–7026.  https://doi.org/10.1074/jbc.M209537200 CrossRefPubMedGoogle Scholar
  32. 32.
    Romero-Pozuelo J, Dason JS, Atwood HL, Ferrús A (2007) Chronic and acute alterations in the functional levels of Frequenins 1 and 2 reveal their roles in synaptic transmission and axon terminal morphology. Eur J Neurosci 26:2428–2443.  https://doi.org/10.1111/j.1460-9568.2007.05877.x CrossRefPubMedGoogle Scholar
  33. 33.
    Chen XL, Zhong ZG, Yokoyama S, Bark C, Meister B, Berggren PO, Roder J, Higashida H et al (2001) Overexpression of rat neuronal calcium sensor-1 in rodent NG108-15 cells enhances synapse formation and transmission. J Physiol 532:649–659.  https://doi.org/10.1111/j.1469-7793.2001.0649e.x CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Tsujimoto T, Jeromin A, Saitoh N, Roder JC, Takahashi T (2002) Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295:2276–2279.  https://doi.org/10.1126/science.1068278 CrossRefPubMedGoogle Scholar
  35. 35.
    Yan J, Leal K, Magupalli VG, Nanou E, Martinez GQ, Scheuer T, Catterall WA (2014) Modulation of Cav2.1 channels by neuronal calcium sensor-1 induces short-term synaptic facilitation. Mol Cell Neurosci 63:124–131.  https://doi.org/10.1016/j.mcn.2014.11.001 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Lian LY, Pandalaneni SR, Todd PAC, Martin VM, Burgoyne RD, Haynes LP (2014) Demonstration of binding of neuronal calcium sensor-1 to the Cav2.1 P/Q-type calcium channel. Biochemistry 53:6052–6062.  https://doi.org/10.1021/bi500568v CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Dent EW, Gertler FB (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209–227.  https://doi.org/10.1016/S0896-6273(03)00633-0 CrossRefPubMedGoogle Scholar
  38. 38.
    Iketani M, Imaizumi C, Nakamura F, Jeromin A, Mikoshiba K, Goshima Y, Takei K (2009) Regulation of neurite outgrowth mediated by neuronal calcium sensor-1 and inositol 1,4,5-trisphosphate receptor in nerve growth cones. Neuroscience 161:743–752.  https://doi.org/10.1016/j.neuroscience.2009.04.019 CrossRefPubMedGoogle Scholar
  39. 39.
    Song H, Poo M (1999) Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol 9:355–363.  https://doi.org/10.1016/S0959-4388(99)80052-X CrossRefPubMedGoogle Scholar
  40. 40.
    Hui H, McHugh D, Hannan M, Zeng F, Xu SZ, Khan SUH, Levenson R, Beech DJ et al (2006) Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J Physiol 572:165–172.  https://doi.org/10.1113/jphysiol.2005.102889 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Tojima T, Hines JH, Henley JR, Kamiguchi H (2011) Second messengers and membrane trafficking direct and organize growth cone steering. Nat Rev Neurosci 12:191–203.  https://doi.org/10.1038/nrn2996 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Wang GX, Poo MM (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434:898–904.  https://doi.org/10.1038/nature03478 CrossRefPubMedGoogle Scholar
  43. 43.
    Gomez TM, Zheng JQ (2006) The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7:115–125.  https://doi.org/10.1038/nrn1844 CrossRefPubMedGoogle Scholar
  44. 44.
    Hui K, Fei G-H, Saab BJ, Su J, Roder JC, Feng ZP (2007) Neuronal calcium sensor-1 modulation of optimal calcium level for neurite outgrowth. Development 134:4479–4489.  https://doi.org/10.1242/dev.008979 CrossRefPubMedGoogle Scholar
  45. 45.
    Hui K, Feng ZP (2008) NCS-1 differentially regulates growth cone and somata calcium channels in Lymnaea neurons. Eur J Neurosci 27:631–643.  https://doi.org/10.1111/j.1460-9568.2008.06023.x CrossRefPubMedGoogle Scholar
  46. 46.
    Sippy T, Cruz-Martín A, Jeromin A, Schweizer FE (2003) Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nat Neurosci 6:1031–1038.  https://doi.org/10.1038/nn1117 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Nanou E, Sullivan JM, Scheuer T, Catterall WA (2016) Calcium sensor regulation of the Cav2.1 Ca2+ channel contributes to short-term synaptic plasticity in hippocampal neurons. Proc Natl Acad Sci U S A 113:1062–1067.  https://doi.org/10.1073/pnas.1524636113 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Brackmann M, Zhao C, Kuhl D, Manahan-Vaughan D, Braunewell KH (2004) MGluRs regulate the expression of neuronal calcium sensor proteins NCS-1 and VILIP-1 and the immediate early gene arg3.1/arc in the hippocampus in vivo. Biochem Biophys Res Commun 322:1073–1079.  https://doi.org/10.1016/j.bbrc.2004.08.028 CrossRefPubMedGoogle Scholar
  49. 49.
    Jo J, Heon S, Kim MJ, Son GH, Park Y, Henley JM, Weiss JL, Sheng M et al (2008) Metabotropic glutamate receptor-mediated LTD involves two interacting Ca2+ sensors, NCS-1 and PICK1. Neuron 60:1095–1111.  https://doi.org/10.1016/j.neuron.2008.10.050 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Génin A, Davis S, Meziane H, Doyère V, Jeromin A, Roder J, Mallet J, Laroche S (2001) Regulated expression of the neuronal calcium sensor-1 gene during long-term potentiation in the dentate gyrus in vivo. Neuroscience 106:571–577.  https://doi.org/10.1016/S0306-4522(01)00301-3 CrossRefPubMedGoogle Scholar
  51. 51.
    Morris RGM, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774–776.  https://doi.org/10.1038/324227a0 CrossRefGoogle Scholar
  52. 52.
    Davis S, Butcher SP, Morris RGM (1992) The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J Neurosci 12:21–34.  https://doi.org/10.1523/JNEUROSCI.12-01-00021.1992 CrossRefPubMedGoogle Scholar
  53. 53.
    Bannerman DM, Good MA, Butcher SP, Ramsay M, Morris RGM (1995) Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378:182–186.  https://doi.org/10.1038/378182a0 CrossRefPubMedGoogle Scholar
  54. 54.
    Sakimura K, Kutsuwada T, Ito I, Manabe T, Takayama C, Kushiya E, Yagi T, Aizawa S et al (1995) Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor ℰ1 subunit. Nature 373:151–155.  https://doi.org/10.1038/373151a0 CrossRefPubMedGoogle Scholar
  55. 55.
    Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711.  https://doi.org/10.1146/annurev.neuro.23.1.649 CrossRefPubMedGoogle Scholar
  56. 56.
    Basu J, Siegelbaum SA (2015) The corticohippocampal circuit, synaptic plasticity, and memory. Cold Spring Harb Perpect Biol 7:a021733.  https://doi.org/10.1101/cshperspect.a021733 CrossRefGoogle Scholar
  57. 57.
    Gomez M, Castro E, Guarin E et al (2001) Ca2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 30:241–248.  https://doi.org/10.1016/S0896-6273(01)00276-8 CrossRefPubMedGoogle Scholar
  58. 58.
    Saab BJ, Georgiou J, Nath A, Lee FJS, Wang M, Michalon A, Liu F, Mansuy IM et al (2009) NCS-1 in the dentate gyrus promotes exploration, synaptic plasticity, and rapid acquisition of spatial memory. Neuron 63:643–656.  https://doi.org/10.1016/j.neuron.2009.08.014 CrossRefPubMedGoogle Scholar
  59. 59.
    Nakamura TY, Nakao S, Nakajo Y, Takahashi JC, Wakabayashi S, Yanamoto H (2017) Possible signaling pathways mediating neuronal calcium sensor-1-dependent spatial learning and memory in mice. PLoS One 12:e0170829.  https://doi.org/10.1371/journal.pone.0170829 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Yanamoto H, Miyamoto S, Nakajo Y, Nakano Y, Hori T, Naritomi H, Kikuchi H (2008) Repeated application of an electric field increases BDNF in the brain, enhances spatial learning, and induces infarct tolerance. Brain Res 1212:79–88.  https://doi.org/10.1016/j.brainres.2008.03.011 CrossRefPubMedGoogle Scholar
  61. 61.
    de Rezende VB, Rosa DV, Comim CM, Magno LAV, Rodrigues ALS, Vidigal P, Jeromin A, Quevedo J et al (2014) NCS-1 deficiency causes anxiety and depressive-like behavior with impaired non-aversive memory in mice. Physiol Behav 130:91–98.  https://doi.org/10.1016/j.physbeh.2014.03.005 CrossRefPubMedGoogle Scholar
  62. 62.
    Nikolaus S, Antke C, Beu M, Müller H-W (2010) Cortical GABA, striatal dopamine and midbrain serotonin as the key players in compulsive and anxiety disorders - results from in vivo imaging studies. Rev Neurosci 21:119–139.  https://doi.org/10.1515/REVNEURO.2010.21.2.119 CrossRefPubMedGoogle Scholar
  63. 63.
    de la Mora MP, Gallegos-Cari A, Arizmendi-García Y, Marcellino D, Fuxe K (2010) Role of dopamine receptor mechanisms in the amygdaloid modulation of fear and anxiety: structural and functional analysis. Prog Neurobiol 90:198–216.  https://doi.org/10.1016/j.pneurobio.2009.10.010 CrossRefPubMedGoogle Scholar
  64. 64.
    Berk M, Dodd S, Kauer-Sant’Anna M et al (2007) Dopamine dysregulation syndrome: implications for a dopamine hypothesis of bipolar disorder. Acta Psychiatr Scand 116:41–49.  https://doi.org/10.1111/j.1600-0447.2007.01058.x CrossRefGoogle Scholar
  65. 65.
    Dunlop BW, Nemeroff CB (2007) The role of dopamine in the pathophysiology of depression. Arch Gen Psychiatry 64:327–337.  https://doi.org/10.1001/archpsyc.64.3.327 CrossRefPubMedGoogle Scholar
  66. 66.
    Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494.  https://doi.org/10.1038/nrn1406 CrossRefPubMedGoogle Scholar
  67. 67.
    Ng E, Varaschin RK, Su P, Browne CJ, Hermainski J, le Foll B, Pongs O, Liu F et al (2016) Neuronal calcium sensor-1 deletion in the mouse decreases motivation and dopamine release in the nucleus accumbens. Behav Brain Res 301:213–225.  https://doi.org/10.1016/j.bbr.2015.12.037 CrossRefPubMedGoogle Scholar
  68. 68.
    Antunes M, Biala G (2012) The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 13:93–110.  https://doi.org/10.1007/s10339-011-0430-z CrossRefPubMedGoogle Scholar
  69. 69.
    Howes OD, Kapur S (2009) The dopamine hypothesis of schizophrenia: version III - the final common pathway. Schizophr Bull 35:549–562.  https://doi.org/10.1093/schbul/sbp006 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Stone JM, Morrison PD, Pilowsky LS (2007) Glutamate and dopamine dysregulation in schizophrenia – a synthesis and selective review. J Psychopharmacol 21:440–452.  https://doi.org/10.1177/0269881106073126 CrossRefPubMedGoogle Scholar
  71. 71.
    Toda M, Abi-Dargham A (2007) Dopamine hypothesis of schizophrenia: making sense of it all. Curr Psychiatry Rep 9:329–336.  https://doi.org/10.1007/s11920-007-0041-7 CrossRefPubMedGoogle Scholar
  72. 72.
    Abi-Dargham A (2004) Do we still believe in the dopamine hypothesis? New data bring new evidence. Int J Neuropsychopharmacol 7:S1–S5.  https://doi.org/10.1017/S1461145704004110 CrossRefPubMedGoogle Scholar
  73. 73.
    Coyle JT (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26:363–382.  https://doi.org/10.1007/s10571-006-9062-8 CrossRefGoogle Scholar
  74. 74.
    Whitton AE, Treadway MT, Pizzagalli DA (2015) Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Curr Opin Psychiatry 28:7–12.  https://doi.org/10.1097/YCO.0000000000000122 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Cousins DA, Butts K, Young AH (2009) The role of dopamine in bipolar disorder. Bipolar Disord 11:787–806.  https://doi.org/10.1111/j.1399-5618.2009.00760.x CrossRefPubMedGoogle Scholar
  76. 76.
    Negyessy L, Goldman-Rakic PS (2005) Subcellular localization of the dopamine D2 receptor and coexistence with the calcium-binding protein neuronal calcium sensor-1 in the primate prefrontal cortex. J Comp Neurol 488:464–475.  https://doi.org/10.1002/cne.20601 CrossRefPubMedGoogle Scholar
  77. 77.
    Woll MP, De Cotiis DA, Bewley MC et al (2011) Interaction between the D2 dopamine receptor and neuronal calcium sensor-1 analyzed by fluorescence anisotropy. Biochemistry 50:8780–8791.  https://doi.org/10.1021/bi200637e CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Dragicevic E, Poetschke C, Duda J, Schlaudraff F, Lammel S, Schiemann J, Fauler M, Hetzel A et al (2014) Cav1.3 channels control D2-autoreceptor responses via NCS-1 in substantia nigra dopamine neurons. Brain 137:2287–2302.  https://doi.org/10.1093/brain/awu131 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Koh PO, Undie AS, Kabbani N, Levenson R, Goldman-Rakic PS, Lidow MS (2003) Up-regulation of neuronal calcium sensor-1 (NCS-1) in the prefrontal cortex of schizophrenic and bipolar patients. Proc Natl Acad Sci 100:313–317.  https://doi.org/10.1073/pnas.232693499 CrossRefPubMedGoogle Scholar
  80. 80.
    Machado-Vieira R, Manji HK, Zarate CA Jr (2009) The role of lithium in the treatment of bipolar disorder: convergent evidence for neurotrophic effects as a unifying hypothesis. Bipolar Disord 11:92–109.  https://doi.org/10.1111/j.1399-5618.2009.00714.x CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Schlecker C, Boehmerle W, Jeromin A, DeGray B, Varshney A, Sharma Y, Szigeti-Buck K, Ehrlich BE (2006) Neuronal calcium sensor-1 enhancement of InsP3 receptor activity is inhibited by therapeutic levels of lithium. J Clin Invest 116:1668–1674.  https://doi.org/10.1172/JCI22466 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Korchounov A, Meyer MF, Krasnianski M (2010) Postsynaptic nigrostriatal dopamine receptors and their role in movement regulation. J Neural Transm 117:1359–1369.  https://doi.org/10.1007/s00702-010-0454-z CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Guzman JN, Sanchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011–11019.  https://doi.org/10.1523/JNEUROSCI.2519-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Ford CP (2014) The role of D2-autoreceptors in regulating dopamine neuron activity and transmission. Neuroscience 282:13–22.  https://doi.org/10.1016/j.neuroscience.2014.01.025 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Tong Y, Pisani A, Martella G, Karouani M, Yamaguchi H, Pothos EN, Shen J (2009) R1441C mutation in LRRK2 impairs dopaminergic neurotransmission in mice. Proc Natl Acad Sci 106:14622–14627.  https://doi.org/10.1073/pnas.0906334106 CrossRefPubMedGoogle Scholar
  86. 86.
    Kessler RM, Woodward ND, Riccardi P, Li R, Ansari MS, Anderson S, Dawant B, Zald D et al (2009) Dopamine D2 receptor levels in striatum, thalamus, substantia nigra, limbic regions, and cortex in schizophrenic subjects. Biol Psychiatry 65:1024–1031.  https://doi.org/10.1016/j.biopsych.2008.12.029 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET et al (2008) Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 13:267–276.  https://doi.org/10.1038/sj.mp.4002058 CrossRefGoogle Scholar
  88. 88.
    Bahi N, Friocourt G, Carrié A, Graham ME, Weiss JL, Chafey P, Fauchereau F, Burgoyne RD et al (2003) IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with neuronal calcium sensor-1 and regulates exocytosis. Hum Mol Genet 12:1415–1425.  https://doi.org/10.1093/hmg/ddg147 CrossRefPubMedGoogle Scholar
  89. 89.
    Yamagata A, Yoshida T, Sato Y, Goto-Ito S, Uemura T, Maeda A, Shiroshima T, Iwasawa-Okamoto S et al (2015) Mechanisms of splicing-dependent trans-synaptic adhesion by PTPδ-IL1RAPL1/IL-1RAcP for synaptic differentiation. Nat Commun 6:1–11.  https://doi.org/10.1038/ncomms7926 CrossRefGoogle Scholar
  90. 90.
    Yoshida T, Yasumura M, Uemura T, Lee SJ, Ra M, Taguchi R, Iwakura Y, Mishina M (2011) IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase δ. J Neurosci 31:13485–13499.  https://doi.org/10.1523/JNEUROSCI.2136-11.2011 CrossRefPubMedGoogle Scholar
  91. 91.
    Valnegri P, Montrasio C, Brambilla D, Ko J, Passafaro M, Sala C (2011) The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTPδ and RhoGAP2. Hum Mol Genet 20(24):4797–4809.  https://doi.org/10.1093/hmg/ddr418
  92. 92.
    Hayashi T, Yoshida T, Ra M, Taguchi R, Mishina M (2013) IL1RAPL1 associated with mental retardation and autism regulates the formation and stabilization of glutamatergic synapses of cortical neurons through RhoA signaling pathway. PLoS One 8:e66254.  https://doi.org/10.1371/journal.pone.0066254 CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Pavlowsky A, Zanchi A, Pallotto M, Giustetto M, Chelly J, Sala C, Billuart P (2010) Neuronal JNK pathway activation by IL-1 is mediated through IL1RAPL1, a protein required for development of cognitive functions. Commun Integr Biol 3:245–247.  https://doi.org/10.4161/cib.3.3.11414 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Pavlowsky A, Gianfelice A, Pallotto M, Zanchi A, Vara H, Khelfaoui M, Valnegri P, Rezai X et al (2010) A postsynaptic signaling pathway that may account for the cognitive defect due to IL1RAPL1 mutation. Curr Biol 20:103–115.  https://doi.org/10.1016/j.cub.2009.12.030 CrossRefPubMedGoogle Scholar
  95. 95.
    Yasumura M, Yoshida T, Yamazaki M, Abe M, Natsume R, Kanno K, Uemura T, Takao K et al (2014) IL1RAPL1 knockout mice show spine density decrease, learning deficiency, hyperactivity and reduced anxiety-like behaviours. Sci Rep 4:1–12.  https://doi.org/10.1038/srep06613 CrossRefGoogle Scholar
  96. 96.
    Gambino F, Kneib M, Pavlowsky A, Skala H, Heitz S, Vitale N, Poulain B, Khelfaoui M et al (2009) IL1RAPL1 controls inhibitory networks during cerebellar development in mice. Eur J Neurosci 30:1476–1486.  https://doi.org/10.1111/j.1460-9568.2009.06975.x CrossRefPubMedGoogle Scholar
  97. 97.
    Montani C, Ramos-Brossier M, Ponzoni L, Gritti L, Cwetsch AW, Braida D, Saillour Y, Terragni B et al (2017) The X-linked intellectual disability protein IL1RAPL1 regulates dendrite complexity. J Neurosci 37:6606–6627.  https://doi.org/10.1523/JNEUROSCI.3775-16.2017 CrossRefPubMedGoogle Scholar
  98. 98.
    Yoshida T, Mishina M (2008) Zebrafish orthologue of mental retardation protein IL1RAPL1 regulates presynaptic differentiation. Mol Cell Neurosci 39:218–228.  https://doi.org/10.1016/j.mcn.2008.06.013 CrossRefPubMedGoogle Scholar
  99. 99.
    Tabolacci E, Pomponi MG, Pietrobono R, Terracciano A, Chiurazzi P, Neri G (2006) A truncating mutation in the IL1RAPL1 gene is responsible for X-linked mental retardation in the MRX21 family. Am J Med Genet 143A:482–487.  https://doi.org/10.1002/ajmg.a.31107 CrossRefGoogle Scholar
  100. 100.
    Nawara M, Klapecki J, Borg K, Jurek M, Moreno S, Tryfon J, Bal J, Chelly J et al (2008) Novel mutation of IL1RAPL1 gene in a nonspecific X-linked mental retardation (MRX) family. Am J Med Genet Part A 146A:3167–3172.  https://doi.org/10.1002/ajmg.a.32613 CrossRefPubMedGoogle Scholar
  101. 101.
    Bhat SS, Ladd S, Grass F, Spence JE, Brasington CK, Simensen RJ, Schwartz CE, DuPont B et al (2008) Disruption of the IL1RAPL1 gene associated with a pericentromeric inversion of the X chromosome in a patient with mental retardation and autism. Clin Genet 73:94–96.  https://doi.org/10.1111/j.1399-0004.2007.00920.x CrossRefPubMedGoogle Scholar
  102. 102.
    Franek KJ, Butler J, Johnson J, Simensen R, Friez MJ, Bartel F, Moss T, DuPont B et al (2011) Deletion of the immunoglobulin domain of IL1RAPL1 results in nonsyndromic X-linked intellectual disability associated with behavioral problems and mild dysmorphism. Am J Med Genet Part A 155:1109–1114.  https://doi.org/10.1002/ajmg.a.33833 CrossRefGoogle Scholar
  103. 103.
    Behnecke A, Hinderhofer K, Bartsch O, Nümann A, Ipach ML, Damatova N, Haaf T, Dufke A et al (2011) Intragenic deletions of IL1RAPL1: report of two cases and review of the literature. Am J Med Genet Part A 155:372–379.  https://doi.org/10.1002/ajmg.a.33656 CrossRefGoogle Scholar
  104. 104.
    Youngs EL, Henkhaus R, Hellings JA, Butler MG (2012) IL1RAPL1 gene deletion as a cause of X-linked intellectual disability and dysmorphic features. Eur J Med Genet 55:32–36.  https://doi.org/10.1016/j.ejmg.2011.08.004 CrossRefPubMedGoogle Scholar
  105. 105.
    Ropers H-H, Hamel BCJ (2005) X-linked mental retardation. Nat Rev Genet 6:46–57.  https://doi.org/10.1038/nrg1501 CrossRefPubMedGoogle Scholar
  106. 106.
    Gambino F, Pavlowsky A, Béglé A et al (2007) IL1-receptor accessory protein-like 1 (IL1RAPL1), a protein involved in cognitive functions, regulates N-type Ca2+-channel and neurite elongation. Proc Natl Acad Sci 104:9063–9068.  https://doi.org/10.1073/pnas.0701133104 CrossRefPubMedGoogle Scholar
  107. 107.
    Romero-Pozuelo J, Dason JS, Mansilla A, Banos-Mateos S, Sardina JL, Chaves-Sanjuan A, Jurado-Gomez J, Santana E et al (2014) The guanine-exchange factor Ric8a binds to the Ca2+ sensor NCS-1 to regulate synapse number and neurotransmitter release. J Cell Sci 127:4246–4259.  https://doi.org/10.1242/jcs.152603 CrossRefPubMedGoogle Scholar
  108. 108.
    Garber KB, Visootsak J, Warren ST (2008) Fragile X syndrome. Eur J Hum Genet 16:666–672.  https://doi.org/10.1038/ejhg.2008.61 CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Mansilla A, Chaves-Sanjuan A, Campillo NE, Semelidou O, Martínez-González L, Infantes L, González-Rubio JM, Gil C et al (2017) Interference of the complex between NCS-1 and Ric8a with phenothiazines regulates synaptic function and is an approach for fragile X syndrome. Proc Natl Acad Sci 114:E999–E1008.  https://doi.org/10.1073/pnas.1611089114 CrossRefPubMedGoogle Scholar
  110. 110.
    Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703–713.  https://doi.org/10.1038/nrn1195 CrossRefPubMedGoogle Scholar
  111. 111.
    Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209:294–301.  https://doi.org/10.1016/j.expneurol.2007.05.014 CrossRefPubMedGoogle Scholar
  112. 112.
    Silver J, Schwab ME, Popovich PG (2015) Central nervous system regenerative failure: role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harb Perspect Biol 7:a020602.  https://doi.org/10.1101/cshperspect.a020602 CrossRefPubMedCentralGoogle Scholar
  113. 113.
    van Niekerk EA, Tuszynski MH, Lu P, Dulin JN (2016) Molecular and cellular mechanisms of axonal regeneration after spinal cord injury. Mol Cell Proteomics 15:394–408.  https://doi.org/10.1074/mcp.R115.053751 CrossRefPubMedGoogle Scholar
  114. 114.
    Tran AP, Warren PM, Silver J (2018) The biology of regeneration failure and success after spinal cord injury. Physiol Rev 98:881–917.  https://doi.org/10.1152/physrev.00017.2017 CrossRefPubMedGoogle Scholar
  115. 115.
    Nakamura TY, Jeromin A, Smith G, Kurushima H, Koga H, Nakabeppu Y, Wakabayashi S, Nabekura J (2006) Novel role of neuronal Ca2+ sensor-1 as a survival factor up-regulated in injured neurons. J Cell Biol 172:1081–1091.  https://doi.org/10.1083/jcb.200508156 CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Yip PK, Wong LF, Sears TA, Yáñez-Muñoz RJ, McMahon SB (2010) Cortical overexpression of neuronal calcium sensor-1 induces functional plasticity in spinal cord following unilateral pyramidal tract injury in rat. PLoS Biol 8:e1000399.  https://doi.org/10.1371/journal.pbio.1000399 CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Mameli M, Balland B, Luján R, Lüscher C (2007) Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317:530–533.  https://doi.org/10.1126/science.1142365 CrossRefPubMedGoogle Scholar
  118. 118.
    Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in mGluR-dependent long-term depression. Science 288:1254–1256.  https://doi.org/10.1126/science.288.5469.1254 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Physiology, Faculty of MedicineUniversity of TorontoTorontoCanada

Personalised recommendations