PRRT2: from Paroxysmal Disorders to Regulation of Synaptic Function

Trends in Neurosciences

Volumn 39, Issue 10, 2016, Pages 668-679

  Valtorta, Flavia ^a   Benfenati, Fabio ^b,c   Zara, Federico ^d   Meldolesi, Jacopo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^d G GASLINI INSTITUTE   (Italy)

Author keywords

dyskinesia; epilepsy; neuronal development; synaptic transmission; synaptopathies

Indexed keywords

CALCIUM; CELL MEMBRANE PROTEIN; INTRACELLULAR CALCIUM SENSING PROTEIN; NEUROTRANSMITTER; PROLINE RICH PROTEIN; PROLINE RICH TRANSMEMBRANE PROTEIN 2; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; NERVE PROTEIN; PRRT2 PROTEIN, HUMAN; PRRT2 PROTEIN, MOUSE;

CALCIUM CELL LEVEL; CELL MIGRATION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC RISK; HUMAN; MOLECULAR PATHOLOGY; NERVE CELL; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PAROXYSMAL DISORDER; PHYSICAL DISEASE BY ETIOLOGY AND PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SYNAPSE; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; SYNAPTOPATHY; ANIMAL; EXOCYTOSIS; GENETICS; METABOLISM; MUTATION; PHENOTYPE;

ANIMALS; EXOCYTOSIS; HUMANS; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PHENOTYPE; SYNAPTIC TRANSMISSION;

EID: 84989165796     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2016.08.005     Document Type: Review

References (65)

1. 1 Stelzl, U., et al. A human protein–protein interaction network: a resource for annotating the proteome. Cell 122 (2005), 957–968.
2. 2 Chen, W.J., et al. Exome sequencing identifies truncating mutations in PRRT2 that cause paroxysmal kinesigenic dyskinesia. Nat. Genet. 43 (2011), 1252–1255.
3. 3 Wang, J.L., et al. Identification of PRRT2 as the causative gene of paroxysmal kinesigenic dyskinesias. Brain 134 (2011), 3493–3501.
4. 4 Kato, N., et al. Paroxysmal kinesigenic choreoathetosis: from first discovery in 1892 to genetic linkage with benign familial infantile convulsions. Epilepsy Res. 70:Suppl 1 (2006), S174–S184.
5. 5 Wood, H., Genetics: expanding the spectrum of neurological disorders associated with PRRT2 mutations. Nat. Rev. Neurol., 8, 2012, 657.
6. 6 Heron, S.E., Dibbens, L.M., Role of PRRT2 in common paroxysmal neurological disorders: a gene with remarkable pleiotropy. J. Med. Genet. 50 (2013), 133–139.
7. 7 Ebrahimi-Fakhari, D., et al. The evolving spectrum of PRRT2-associated paroxysmal diseases. Brain 138 (2015), 3476–3495.
8. 8 Li, M., et al. PRRT2 mutant leads to dysfunction of glutamate signaling. Int. J. Mol. Sci. 16 (2015), 9134–9151.
9. 9 Ebrahimi-Fakhari, D., et al. Child Neurology: PRRT2-associated movement disorders and differential diagnoses. Neurology 83 (2014), 1680–1683.
10. 10 Rossi, P., et al. A novel topology of proline-rich transmembrane protein 2 (PRRT2): hints for an intracellular function at the synapse. J. Biol. Chem. 291 (2016), 6111–6123.
11. 11 Valente, P., et al. PRRT2 is a key component of the Ca(2 + )-dependent neurotransmitter release machinery. Cell Rep. 15 (2016), 117–131.
12. 12 Liu, X.R., et al. Paroxysmal hypnogenic dyskinesia is associated with mutations in the PRRT2 gene. Neurol. Genet., 2, 2016, e66.
13. 13 Liu, Y.T., et al. PRRT2 mutations lead to neuronal dysfunction and neurodevelopmental defects. Oncotarget, 2016 Published online May 9, 2016. http://dx.doi.org/10.18632/oncotarget.9258.
14. 14 Gardiner, A.R., et al. The clinical and genetic heterogeneity of paroxysmal dyskinesias. Brain 138 (2015), 3567–3580.
15. 15 Cloarec, R., et al. PRRT2 links infantile convulsions and paroxysmal dyskinesia with migraine. Neurology 79 (2012), 2097–2103.
16. 16 Lee, Y.C., et al. PRRT2 mutations in paroxysmal kinesigenic dyskinesia with infantile convulsions in a Taiwanese cohort. PLoS One, 7, 2012, e38543.
17. 17 Lee, H.Y., et al. Mutations in the gene PRRT2 cause paroxysmal kinesigenic dyskinesia with infantile convulsions. Cell Rep. 1 (2012), 2–12.
18. 18 Ono, S., et al. Mutations in PRRT2 responsible for paroxysmal kinesigenic dyskinesias also cause benign familial infantile convulsions. J. Hum. Genet. 57 (2012), 338–341.
19. 19 Meneret, A., et al. PRRT2 mutations and paroxysmal disorders. Eur. J. Neurol. 20 (2013), 872–878.
20. 20 Riant, F., et al. PRRT2 mutations cause hemiplegic migraine. Neurology 79 (2012), 2122–2124.
21. 21 Becker, F., et al. PRRT2-related disorders: further PKD and ICCA cases and review of the literature. J. Neurol. 260 (2013), 1234–1244.
22. 22 Kumar, K.R., et al. Genetics of Parkinson disease and other movement disorders. Curr. Opin. Neurol. 25 (2012), 466–474.
23. 23 Brueckner, F., et al. Unusual variability of PRRT2 linked phenotypes within a family. Eur. J. Paediatr. Neurol. 18 (2014), 540–542.
24. 24 Delcourt, M., et al. Severe phenotypic spectrum of biallelic mutations in PRRT2 gene. J. Neurol. Neurosurg. Psychiatry 86 (2015), 782–785.
25. 25 Labate, A., et al. Homozygous c.649dupC mutation in PRRT2 worsens the BFIS/PKD phenotype with mental retardation, episodic ataxia, and absences. Epilepsia 53 (2012), e196–e199.
26. 26 Shinawi, M., et al. Recurrent reciprocal 16p11.2 rearrangements associated with global developmental delay, behavioural problems, dysmorphism, epilepsy, and abnormal head size. J. Med. Genet. 47 (2010), 332–341.
27. 27 Weiss, L.A., et al. Association between microdeletion and microduplication at 16p11.2 and autism. N. Engl. J. Med. 358 (2008), 667–675.
28. 28 Sallman Almen, M., et al. The dispanins: a novel gene family of ancient origin that contains 14 human members. PLoS One, 7, 2012, e31961.
29. 29 Heron, S.E., et al. PRRT2 mutations cause benign familial infantile epilepsy and infantile convulsions with choreoathetosis syndrome. Am. J. Hum. Genet. 90 (2012), 152–160.
30. 30 Trabzuni, D., et al. Quality control parameters on a large dataset of regionally dissected human control brains for whole genome expression studies. J. Neurochem. 119 (2011), 275–282.
31. 31 Garcia-Manteiga, J.M., et al. REST-governed gene expression profiling in a neuronal cell model reveals novel direct and indirect processes of repression and up-regulation. Front. Cell. Neurosci., 9, 2015, 438.
32. 32 Sudhof, T.C., Rizo, J., Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol., 3, 2011 a005637.
33. 33 de Vries, B., et al. PRRT2 mutation causes benign familial infantile convulsions. Neurology 79 (2012), 2154–2155.
34. 34 Luo, C., et al. Altered intrinsic brain activity in patients with paroxysmal kinesigenic dyskinesia by PRRT2 mutation: altered brain activity by PRRT2 mutation. Neurol. Sci. 34 (2013), 1925–1931.
35. 35 Boyken, J., et al. Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78 (2013), 285–297.
36. 36 Schwenk, J., et al. Regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain. Neuron 84 (2014), 41–54.
37. 37 Shanks, N.F., et al. Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L. Cell Rep. 1 (2012), 590–598.
38. 38 Geppert, M., et al. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79 (1994), 717–727.
39. 39 Pang, Z.P., et al. Synaptotagmin-2 is essential for survival and contributes to Ca2+ triggering of neurotransmitter release in central and neuromuscular synapses. J. Neurosci. 26 (2006), 13493–13504.
40. 40 Sun, J., et al. A dual-Ca2 + -sensor model for neurotransmitter release in a central synapse. Nature 450 (2007), 676–682.
41. 41 Fox, M.A., Sanes, J.R., Synaptotagmin I and II are present in distinct subsets of central synapses. J. Comp. Neurol. 503 (2007), 280–296.
42. 42 Kerr, A.M., et al. Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 15581–15586.
43. 43 Shen, Y., et al. Protein mutated in paroxysmal dyskinesia interacts with the active zone protein RIM and suppresses synaptic vesicle exocytosis. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 2935–2941.
44. 44 Kaeser, P.S., et al. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144 (2011), 282–295.
45. 45 Hibino, H., et al. RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2 + ) channels. Neuron 34 (2002), 411–423.
46. 46 Catterall, W.A., Few, A.P., Calcium channel regulation and presynaptic plasticity. Neuron 59 (2008), 882–901.
47. 47 Condliffe, S.B., et al. Endogenous SNAP-25 regulates native voltage-gated calcium channels in glutamatergic neurons. J. Biol. Chem. 285 (2010), 24968–24976.
48. 48 Rohena, L., et al. Mutation in SNAP25 as a novel genetic cause of epilepsy and intellectual disability. Rare Dis., 1, 2013, e26314.
49. 49 Zhang, Y., et al. Elevated thalamic low-voltage-activated currents precede the onset of absence epilepsy in the SNAP25-deficient mouse mutant coloboma. J. Neurosci. 24 (2004), 5239–5248.
50. 50 Corradini, I., et al. Epileptiform activity and cognitive deficits in SNAP-25(+/-) mice are normalized by antiepileptic drugs. Cereb. Cortex 24 (2014), 364–376.
51. 51 Wein, T., et al. Exquisite sensitivity of paroxysmal kinesigenic choreoathetosis to carbamazepine. Neurology 47 (1996), 1104–1106.
52. 52 Zhang, S.Z., et al. Urine-derived induced pluripotent stem cells as a modeling tool for paroxysmal kinesigenic dyskinesia. Biol. Open 4 (2015), 1744–1752.
53. 53 Li, C., et al. Aberrant transcriptional networks in step-wise neurogenesis of paroxysmal kinesigenic dyskinesia-induced pluripotent stem cells. Oncotarget, 2016 Published online July 18, 2016. http://dx.doi.org/10.18632/oncotarget.10680.
54. 54 Casillas-Espinosa, P.M., et al. Regulators of synaptic transmission: roles in the pathogenesis and treatment of epilepsy. Epilepsia 53:Suppl 9 (2012), 41–58.
55. 55 Staley, K., Molecular mechanisms of epilepsy. Nat. Neurosci. 18 (2015), 367–372.
56. 56 Jahn, R., Fasshauer, D., Molecular machines governing exocytosis of synaptic vesicles. Nature 490 (2012), 201–207.
57. 57 Sudhof, T.C., Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80 (2013), 675–690.
58. 58 Rizo, J., Xu, J., The synaptic vesicle release machinery. Annu. Rev. Biophys. 44 (2015), 339–367.
59. 59 Gundelfinger, E.D., et al. Role of bassoon and piccolo in assembly and molecular organization of the active zone. Front. Synaptic Neurosci., 7, 2015, 19.
60. 60 Ryan, D.P., Ptacek, L.J., Episodic neurological channelopathies. Neuron 68 (2010), 282–292.
61. 61 Takamori, S., et al. Molecular anatomy of a trafficking organelle. Cell 127 (2006), 831–846.
62. 62 Bayes, A., et al. Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat. Neurosci. 14 (2011), 19–21.
63. 63 Li, J.Y., et al. Huntington's disease: a synaptopathy?. Trends Mol. Med. 9 (2003), 414–420.
64. 64 Grant, S.G., Synaptopathies: diseases of the synaptome. Curr. Opin. Neurobiol. 22 (2012), 522–529.
65. 65 Chiappalone, M., et al. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb. Cortex 19 (2009), 1422–1439.