PRRT2 mutant leads to dysfunction of glutamate signaling

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 9134-9151

  Li, Ming ^a   Niu, Fenghe ^a   Zhu, Xilin ^a   Wu, Xiaopan ^a   Shen, Ning ^a   Peng, Xiaozhong ^a   Liu, Ying ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

Glutamate; GRIA1; PRRT2; SNAP25

Indexed keywords

AMPA RECEPTOR; ASPARTIC ACID; GLUTAMIC ACID; GLYCINE; MEMBRANE PROTEIN; MESSENGER RNA; POSTSYNAPTIC DENSITY PROTEIN 95; PROLINE RICH TRANSMEMBRANE PROTEIN 2; UNCLASSIFIED DRUG; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; GLUTAMIC ACID DERIVATIVE; NERVE PROTEIN; PROTEIN BINDING; PRRT2 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOREOATHETOSIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PAROXYSMAL KINESIGENIC CHOREOATHETOSIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADOLESCENT; ANIMAL; CASE CONTROL STUDY; CELL CULTURE; CELL LINE; CELL MEMBRANE; CHILD; DYSTONIA; GENE INACTIVATION; GENETICS; METABOLISM; MUTATION; NERVE CELL; ONSET AGE; YOUNG ADULT;

ADOLESCENT; ADULT; AGE OF ONSET; ANIMALS; ASPARTIC ACID; CASE-CONTROL STUDIES; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; CHILD; DYSTONIA; FEMALE; GENE KNOCKOUT TECHNIQUES; GLUTAMATES; GLYCINE; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MUTATION; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BINDING; RECEPTORS, AMPA; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 84928405610     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16059134     Document Type: Article

References (59)

1. Kertesz, A. Paroxysmal kinesigenic choreoathetosis. An entity within the paroxysmal choreoathetosis syndrome. Description of 10 cases, including 1 autopsied. Neurology 1967, 17, 680–690.
2. Bruno, M.K.; Hallett, M.; Gwinn-Hardy, K.; Sorensen, B.; Considine, E.; Tucker, S.; Lynch, D.R.; Mathews, K.D.; Swoboda, K.J.; Harris, J. et al. Clinical evaluation of idiopathic paroxysmal kinesigenic dyskinesia: New diagnostic criteria. Neurology 2004, 63, 2280–2287.
3. Li, J.; Zhu, X.; Wang, X.; Sun, W.; Feng, B.; Du, T.; Sun, B.; Niu, F.; Wei, H.; Wu, X. et al. Targeted genomic sequencing identifies PRRT2 mutations as a cause of paroxysmal kinesigenic choreoathetosis. J. Med. Genet. 2012, 49, 76–78.
4. Chen, W.J.; Lin, Y.; Xiong, Z.Q.; Wei, W.; Ni, W.; Tan, G.H.; Guo, S.L.; He, J.; Chen, Y.F.; Zhang, Q.J. et al. Exome sequencing identifies truncating mutations in PRRT2 that cause paroxysmal kinesigenic dyskinesia. Nat. Genet. 2011, 43, 1252–1255.
5. Wang, J.L.; Cao, L.; Li, X.H.; Hu, Z.M.; Li, J.D.; Zhang, J.G.; Liang, Y.; San, A.; Li, N.; Chen, S.Q. et al. Identification of PRRT2 as the causative gene of paroxysmal kinesigenic dyskinesias. Brain 2011, 134, 3493–3501.
6. Lee, H.Y.; Huang, Y.; Bruneau, N.; Roll, P.; Roberson, E.D.; Hermann, M.; Quinn, E.; Maas, J.; Edwards, R.; Ashizawa, T. et al. Mutations in the gene PRRT2 cause paroxysmal kinesigenic dyskinesia with infantile convulsions. Cell. Rep. 2012, 1, 2–12.
7. Heron, S.E.; Grinton, B.E.; Kivity, S.; Afawi, Z.; Zuberi, S.M.; Hughes, J.N.; Pridmore, C.; Hodgson, B.L.; Iona, X.; Sadleir, L.G. et al. PRRT2 mutations cause benign familial infantile epilepsy and infantile convulsions with choreoathetosis syndrome. Am. J. Hum. Genet. 2012, 90, 152–160.
8. Yang, Y.; Xia, Z.; Liu, Y. SNAP-25 functional domains in SNARE core complex assembly and glutamate release of cerebellar granule cells. J. Biol. Chem. 2000, 275, 29482–29487.
9. Verderio, C.; Pozzi, D.; Pravettoni, E.; Inverardi, F.; Schenk, U.; Coco, S.; Proux-Gillardeaux, V.; Galli, T.; Rossetto, O.; Frassoni, C. et al. SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 2004, 41, 599–610.
10. Garbelli, R.; Inverardi, F.; Medici, V.; Amadeo, A.; Verderio, C.; Matteoli, M.; Frassoni, C. Heterogeneous expression of SNAP-25 in rat and human brain. J. Comp. Neurol. 2008, 506, 373–386.
11. Mandolesi, G.; Vanni, V.; Cesa, R.; Grasselli, G.; Puglisi, F.; Cesare, P.; Strata, P. Distribution of the SNAP25 and SNAP23 synaptosomal-associated protein isoforms in rat cerebellar cortex. Neuroscience 2009, 164, 1084–1096.
12. Costantin, L.; Bozzi, Y.; Richichi, C.; Viegi, A.; Antonucci, F.; Funicello, M.; Gobbi, M.; Mennini, T.; Rossetto, O.; Montecucco, C. et al. Antiepileptic effects of botulinum neurotoxin E. J. Neurosci. 2005, 25, 1943–1951.
13. Haglid, K.G.; Wang, S.; Qiner, Y.; Hamberger, A. Excitotoxicity. Experimental correlates to human epilepsy. Mol. Neurobiol. 1994, 9, 259–263.
14. Alam, Z.; Coombes, N.; Waring, R.H.; Williams, A.C.; Steventon, G.B. Plasma levels of neuroexcitatory amino acids in patients with migraine or tension headache. J. Neurol. Sci. 1998, 156, 102–106.
15. Shimmura, C.; Suda, S.; Tsuchiya, K.J.; Hashimoto, K.; Ohno, K.; Matsuzaki, H.; Iwata, K.; Matsumoto, K.; Wakuda, T.; Kameno, Y. et al. Alteration of plasma glutamate and glutamine levels in children with high-functioning autism. PLoS ONE 2011, 6, e25340.
16. Schwenk, J.; Harmel, N.; Brechet, A.; Zolles, G.; Berkefeld, H.; Muller, C.S.; Bildl, W.; Baehrens, D.; Huber, B.; Kulik, A. et al. High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 2012, 74, 621–633.
17. McGale, E.H.; Pye, I.F.; Stonier, C.; Hutchinson, E.C.; Aber, G.M. Studies of the inter-relationship between cerebrospinal fluid and plasma amino acid concentrations in normal individuals. J. Neurochem. 1977, 29, 291–297.
18. Alfredsson, G.; Wiesel, F.A.; Tylec, A. Relationships between glutamate and monoamine metabolites in cerebrospinal fluid and serum in healthy volunteers. Biol. Psychiatry 1988, 23, 689–697.
19. Gerachshenko, T.; Blackmer, T.; Yoon, E.J.; Bartleson, C.; Hamm, H.E.; Alford, S. Gbetagamma acts at the C terminus of SNAP-25 to mediate presynaptic inhibition. Nat. Neurosci. 2005, 8, 597–605.
20. Zhang, J.; Abdullah, J.M. The role of GluA1 in central nervous system disorders. Rev. Neurosci. 2013, 24, 499–505.
21. Almen, M.S.; Bringeland, N.; Fredriksson, R.; Schioth, H.B. The dispanins: A novel gene family of ancient origin that contains 14 human members. PLoS ONE 2012, 7, e31961.
22. Kalashnikova, E.; Lorca, R.A.; Kaur, I.; Barisone, G.A.; Li, B.; Ishimaru, T.; Trimmer, J.S.; Mohapatra, D.P.; Diaz, E. SynDIG1: An activity-regulated, AMPA-receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron 2010, 65, 80–93.
23. Heron, S.E.; Dibbens, L.M. Role of PRRT2 in common paroxysmal neurological disorders: A gene with remarkable pleiotropy. J. Med. Genet. 2013, 50, 133–139.
24. Zheng, W.; Zhang, J.; Deng, X.; Xiao, J.; Yuan, L.; Yang, Y.; Guan, L.; Song, Z.; Yang, Z.; Deng, H. Identification of a premature termination mutation in the Proline-Rich Transmembrane Protein 2 Gene in a Chinese Family with Febrile Seizures. Mol. Neurobiol. 2014, in press.
25. He, Z.W.; Qu, J.; Zhang, Y.; Mao, C.X.; Wang, Z.B.; Mao, X.Y.; Deng, Z.Y.; Zhou, B.T.; Yin, J.Y.; Long, H.Y. et al. PRRT2 Mutations Are related to febrile Seizures in Epileptic Patients. Int. J. Mol. Sci. 2014, 15, 23408–23417.
26. Meneret, A.; Gaudebout, C.; Riant, F.; Vidailhet, M.; Depienne, C.; Roze, E. PRRT2 mutations and paroxysmal disorders. Eur. J. Neurol. 2013, 20, 872–878.
27. Delcourt, M.; Riant, F.; Mancini, J.; Milh, M.; Navarro, V.; Roze, E.; Humbertclaude, V.; Korff, C.; Portes, V.D.; Szepetowski, P. et al. Severe phenotypic spectrum of biallelic mutations in PRRT2 gene. J. Neurol. Neurosurg. Psychiatry 2015, in press.
28. Eid, T.; Thomas, M.J.; Spencer, D.D.; Runden-Pran, E.; Lai, J.C.; Malthankar, G.V.; Kim, J.H.; Danbolt, N.C.; Ottersen, O.P.; Lanerolle, N.C. Loss of glutamine synthetase in the human epileptogenic hippocampus: Possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 2004, 363, 28–37.
29. Cavus, I.; Pan, J.W.; Hetherington, H.P.; Abi-Saab, W.; Zaveri, H.P.; Vives, K.P.; Krystal, J.H.; Spencer, S.S.; Spencer, D.D. Decreased hippocampal volume on MRI is associated with increased extracellular glutamate in epilepsy patients. Epilepsia 2008, 49, 1358–1366.
30. Sirvanci, S.; Meshul, C.K.; Onat, F.; San, T. Immunocytochemical analysis of glutamate and GABA in hippocampus of genetic absence epilepsy rats (GAERS). Brain Res. 2003, 988, 180–188.
31. Podell, M.; Hadjiconstantinou, M. Cerebrospinal fluid gamma-aminobutyric acid and glutamate values in dogs with epilepsy. Am. J. Vet. Res. 1997, 58, 451–456.
32. Creevy, K.E.; Gagnepain, J.F.; Platt, S.R.; Edwards, G.L.; Kent, M. Comparison of concentrations of γ-aminobutyric acid and glutamate in cerebrospinal fluid of dogs with idiopathic epilepsy with and without seizure-related magnetic resonance imaging hyperintense areas in the limbic system. Am. J. Vet. Res. 2013, 74, 1118–1125.
33. Meldrum, B.S. The role of glutamate in epilepsy and other CNS disorders. Neurology 1994, 44, S14–S23.
34. Paraskevas, G.P.; Triantafyllou, N.I.; Kapaki, E.; Limpitaki, G.; Petropoulou, O.; Vassilopoulos, D. Add-on lamotrigine treatment and plasma glutamate levels in epilepsy: Relation to treatment response. Epilepsy Res. 2006, 70, 184–189.
35. Ferrari, M.D.; Odink, J.; Bos, K.D.; Malessy, M.J.; Bruyn, G.W. Neuroexcitatory plasma amino acids are elevated in migraine. Neurology 1990, 40, 1582–1586.
36. Cananzi, A.R.; D’Andrea, G.; Perini, F.; Zamberlan, F.; Welch, K.M. Platelet and plasma levels of glutamate and glutamine in migraine with and without aura. Cephalalgia 1995, 15, 132–135.
37. Gallai, V.; Alberti, A.; Gallai, B.; Coppola, F.; Floridi, A.; Sarchielli, P. Glutamate and nitric oxide pathway in chronic daily headache: Evidence from cerebrospinal fluid. Cephalalgia 2003, 23, 166–174.
38. Peres, M.F.; Zukerman, E.; Senne Soares, C.A.; Alonso, E.O.; Santos, B.F.; Faulhaber, M.H. Cerebrospinal fluid glutamate levels in chronic migraine. Cephalalgia 2004, 24, 735–739.
39. Vieira, D.S.; Naffah-Mazzacoratti Mda, G.; Zukerman, E.; Senne Soares, C.A.; Cavalheiro, E.A.; Peres, M.F. Glutamate levels in cerebrospinal fluid and triptans overuse in chronic migraine. Headache 2007, 47, 842–847.
40. Ferrari, A.; Spaccapelo, L.; Pinetti, D.; Tacchi, R.; Bertolini, A. Effective prophylactic treatments of migraine lower plasma glutamate levels. Cephalalgia 2009, 29, 423–429.
41. Stover, J.F.; Kempski, O.S. Anesthesia increases circulating glutamate in neurosurgical patients. Acta Neurochir. (Wien.) 2005, 147, 847–853.
42. Friedman, A.; Kaufer, D.; Shemer, J.; Hendler, I.; Soreq, H.; Tur-Kaspa, I. Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response. Nat. Med. 1996, 2, 1382–1385.
43. Mayhan, W.G.; Didion, S.P. Glutamate-induced disruption of the blood-brain barrier in rats. Role of nitric oxide. Stroke 1996, 27, 965–969; discussion 970.
44. Lee, H.Y.; Nakayama, J.; Xu, Y.; Fan, X.; Karouani, M.; Shen, Y.; Pothos, E.N.; Hess, E.J.; Fu, Y.H.; Edwards, R.H. et al. Dopamine dysregulation in a mouse model of paroxysmal nonkinesigenic dyskinesia. J. Clin. Investig. 2012, 122, 507–518.
45. Ebrahimi-Fakhari, D.; Kang, K.S.; Kotzaeridou, U.; Kohlhase, J.; Klein, C.; Assmann, B.E. Child Neurology: PRRT2-associated movement disorders and differential diagnoses. Neurology 2014, 83, 1680–1683.
46. Mehta, P.P.; Battenberg, E.; Wilson, M.C. SNAP-25 and synaptotagmin involvement in the final Ca2+-dependent triggering of neurotransmitter exocytosis. Proc. Natl. Acad. Sci. USA 1996, 93, 10471–10476.
47. Antonucci, F.; Cerri, C.; Maya Vetencourt, J.F.; Caleo, M. Acute neuroprotection by the synaptic blocker botulinum neurotoxin E in a rat model of focal cerebral ischaemia. Neuroscience 2010, 169, 395–401.
48. Dolly, J.O.; O’Connell, M.A. Neurotherapeutics to inhibit exocytosis from sensory neurons for the control of chronic pain. Curr. Opin. Pharmacol. 2012, 12, 100–108.
49. Kennard, J.T.; Barmanray, R.; Sampurno, S.; Ozturk, E.; Reid, C.A.; Paradiso, L.; D’Abaco, G.M.; Kaye, A.H.; Foote, S.J.; O’Brien, T.J. et al. Stargazin and AMPA receptor membrane expression is increased in the somatosensory cortex of Genetic Absence Epilepsy Rats from Strasbourg. Neurobiol. Dis. 2011, 42, 48–54.
50. Rajasekaran, K.; Joshi, S.; Kozhemyakin, M.; Todorovic, M.S.; Kowalski, S.; Balint, C.; Kapur, J. Receptor trafficking hypothesis revisited: Plasticity of AMPA receptors during established status epilepticus. Epilepsia 2013, 54, 14–16.
51. Formicola, D.; Aloia, A.; Sampaolo, S.; Farina, O.; Diodato, D.; Griffiths, L.R.; Gianfrancesco, F.; di Iorio, G.; Esposito, T. Common variants in the regulative regions of GRIA1 and GRIA3 receptor genes are associated with migraine susceptibility. BMC Med. Genet. 2010, 11, doi:10.1186/1471-2350-11-103.
52. Faught, E. BGG492 (selurampanel), an AMPA/kainate receptor antagonist drug for epilepsy. Expert Opin. Investig. Drugs 2014, 23, 107–113.
53. Gomez-Mancilla, B.; Brand, R.; Jurgens, T.P.; Gobel, H.; Sommer, C.; Straube, A.; Evers, S.; Sommer, M.; Campos, V.; Kalkman, H.O. et al. Randomized, multicenter trial to assess the efficacy, safety and tolerability of a single dose of a novel AMPA receptor antagonist BGG492 for the treatment of acute migraine attacks. Cephalalgia 2014, 34, 103–113.
54. Li, H.F.; Chen, W.J.; Ni, W.; Wang, K.Y.; Liu, G.L.; Wang, N.; Xiong, Z.Q.; Xu, J.; Wu, Z.Y. PRRT2 mutation correlated with phenotype of paroxysmal kinesigenic dyskinesia and drug response. Neurology 2013, 80, 1534–1535.
55. Dai, Z.; Wu, Z.; Wang, J.; Wang, X.; Jia, S.; Bazer, F.W.; Wu, G. Analysis of polyamines in biological samples by HPLC involving pre-column derivatization with O-phthalaldehyde and N-acetyl-L-cysteine. Amino Acids 2014, 46, 1557–1564.
56. Wang, L.; Huang, Y.; Wu, J.; Lv, G.; Zhou, L.; Jia, J. Effect of Buyang Huanwu decoction on amino acid content in cerebrospinal fluid of rats during ischemic/reperfusion injury. J. Pharm. Biomed. Anal. 2013, 86, 143–150.
57. Li, W.; Shi, L.; You, Y.; Gong, Y.; Yin, B.; Yuan, J.; Peng, X. Downstream of tyrosine kinase/docking protein 6, as a novel substrate of tropomyosin-related kinase C receptor, is involved in neurotrophin 3-mediated neurite outgrowth in mouse cortex neurons. BMC Biol. 2010, 8, doi:10.1186/1741-7007-8-86.
58. Rubinson, D.A.; Dillon, C.P.; Kwiatkowski, A.V.; Sievers, C.; Yang, L.; Kopinja, J.; Rooney, D.L.; Zhang, M.; Ihrig, M.M.; McManus, M.T. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 2003, 33, 401–406.
59. Wang, Z.; Wei, X.; Liu, K.; Zhang, X.; Yang, F.; Zhang, H.; He, Y.; Zhu, T.; Li, F.; Shi, W. et al. NOX2 deficiency ameliorates cerebral injury through reduction of complexin II-mediated glutamate excitotoxicity in experimental stroke. Free Radic. Biol. Med. 2013, 65, 942–951.