TRIO loss of function is associated with mild intellectual disability and affects dendritic branching and synapse function

Human Molecular Genetics

Volumn 25, Issue 5, 2016, Pages 892-902

  Ba, Wei ^a,b   Yan, Yan ^c   Reijnders, Margot R F ^a   Schuurs Hoeijmakers, Janneke H M ^a   Feenstra, Ilse ^a   Bongers, Ernie M H F ^a   Bosch, Daniëlle G M ^a,b,f   De Leeuw, Nicole ^a   Pfundt, Rolph ^a   Gilissen, Christian ^a   De Vries, Petra F ^a   Veltman, Joris A ^a,b,g   Hoischen, Alexander ^a   Mefford, Heather C ^d   Eichler, Evan E ^d,e   Vissers, Lisenka E L M ^a   Kasri, Nael Nadif ^a,b   De Vries, Bert B A ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY   (Netherlands)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f Institute for the Visually Impaired   (Netherlands)

^g MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN G; CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; PROTEIN; SHORT HAIRPIN RNA; TRIO PROTEIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN SERINE THREONINE KINASE; TRIO PROTEIN, HUMAN;

ADULT; AGGRESSION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN DEVELOPMENT; CANONICAL SPLICE SITE; CASE REPORT; CHILD; DENDRITE; DENDRITIC BRANCHING; DOWN REGULATION; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; FRAMESHIFT MUTATION; GENE FREQUENCY; GLUTAMATERGIC SYNAPSE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HUMAN; HUMAN CELL; HYPERACTIVITY; IMMUNOHISTOCHEMISTRY; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; MALE; MISSENSE MUTATION; NERVE FIBER; NERVE FIBER GROWTH; NEXT GENERATION SEQUENCING; NONHUMAN; NONSENSE MUTATION; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RNA SPLICING; SCHOOL CHILD; START CODON; SYNAPSE; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; YOUNG ADULT; ANIMAL; DEFICIENCY; DNA SEQUENCE; GENE EXPRESSION; GENETICS; HIPPOCAMPUS; METABOLISM; MUTATION; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PRIMARY CELL CULTURE; RESTLESSNESS; SEVERITY OF ILLNESS INDEX;

ADULT; ANIMALS; AUTISTIC DISORDER; CHILD; FEMALE; GENE EXPRESSION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; HUMANS; INTELLECTUAL DISABILITY; MALE; MUTATION; NEUROGENESIS; NEURONS; PRIMARY CELL CULTURE; PROTEIN-SERINE-THREONINE KINASES; PSYCHOMOTOR AGITATION; RATS; SEQUENCE ANALYSIS, DNA; SEVERITY OF ILLNESS INDEX; SYNAPSES;

EID: 84962888163     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv618     Document Type: Article

References (51)

1. Leonard, H. and Wen, X. (2002) The epidemiology of mental retardation: challenges and opportunities in the new millennium. Ment. Retard. Dev. Disabil. Res. Rev., 8, 117-134.
2. Vissers, L.E.L.M., Gilissen, C. and Veltman, J.A. (2015) Genetic studies in intellectual disability and related disorders. Nat. Rev. Genet. doi:10.1038/nrg3999.
3. Bamshad, M.J., Ng, S.B., Bigham, A.W., Tabor, H.K., Emond, M.J., Nickerson, D.A. and Shendure, J. (2011) Exome sequencing as a tool for Mendelian disease gene discovery. Nat. Rev. Genet., 12, 745-755.
4. Yang, Y., Muzny, D.M., Reid, J.G., Bainbridge, M.N., Willis, A., Ward, P.A., Braxton, A., Beuten, J., Xia, F., Niu, Z. et al. (2013) Clinical whole-exome sequencing for the diagnosis of Mendelian disorders. N. Engl. J. Med., 369, 1502-1511.
5. Vissers, L.E.L.M., de Ligt, J., Gilissen, C., Janssen, I., Steehouwer, M., de Vries, P., van Lier, B., Arts, P., Wieskamp, N., del Rosario, M. et al. (2010) A de novo paradigm for mental retardation. Nat. Genet., 42, 1109-1112.
6. de Ligt, J., Willemsen, M.H., van Bon, B.W.M., Kleefstra, T., Yntema, H.G., Kroes, T., Vulto-van Silfhout, A.T., Koolen, D.A., de Vries, P., Gilissen, C. et al. (2012) Diagnostic exome sequencing in persons with severe intellectual disability. N. Engl. J. Med., 367, 1921-1929.
7. Rauch, A., Wieczorek, D., Graf, E., Wieland, T., Endele, S., Schwarzmayr, T., Albrecht, B., Bartholdi, D., Beygo, J., Di Donato, N. et al. (2012) Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study. Lancet, 380, 1674-1682.
8. The Deciphering Developmental Disorders Study (2014) Large-scale discovery of novel genetic causes of developmental disorders. Nature, 10.1038/nature14135.
9. Wright, C.F., Fitzgerald, T.W., Jones, W.D., Clayton, S., McRae, J.F., van Kogelenberg, M., King, D.A., Ambridge, K., Barrett, D.M., Bayzetinova, T. et al. (2014) Genetic diagnosis of developmental disorders in the DDD study: a scalable analysis of genome-wide research data. Lancet, doi: 10.1016/S0140-6736 (14)61705-0.
10. Yang, Y., Muzny, D.M., Xia, F., Niu, Z., Person, R., Ding, Y., Ward, P., Braxton, A., Wang, M., Buhay, C. et al. (2014) Molecular findings among patients referred for clinical whole-exome sequencing. JAMA, 312, 1870-1879.
11. Gilissen, C., Hehir-Kwa, J.Y., Thung, D.T., van de Vorst, M., van Bon, B.W.M., Willemsen, M.H., Kwint, M., Janssen, I.M., Hoischen, A., Schenck, A. et al. (2014) Genome sequencing identifies major causes of severe intellectual disability. Nature, 511, 344-347.
12. Vulto-van Silfhout, A.T., Hehir-Kwa, J.Y., van Bon, B.W.M., Schuurs-Hoeijmakers, J.H.M., Meader, S., Hellebrekers, C.J.M., Thoonen, I.J.M., de Brouwer, A.P.M., Brunner, H.G., Webber, C. et al. (2013) Clinical significance of de novo and inherited copy-number variation. Hum. Mutat., 34, 1679-1687.
13. EuroEPINOMICS-RES Consortium, Epilepsy Phenome/Genome ProjectEpi4 K Consortium (2014) De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am. J. Hum. Genet., 95, 360-370.
14. Iossifov, I., O'Roak, B.J., Sanders, S.J., Ronemus, M., Krumm, N., Levy, D., Stessman, H.A., Witherspoon, K.T., Vives, L., Patterson, K.E. et al. (2014) The contribution of de novo coding mutations to autism spectrum disorder. Nature, 515, 216-221.
15. Debant, A., Serra-Pagès, C., Seipel, K., O'Brien, S., Tang, M., Park, S.H. and Streuli, M. (1996) The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc. Natl Acad. Sci. USA, 93, 5466-5471.
16. Medley, Q.G., Serra-Pagès, C., Iannotti, E., Seipel, K., Tang, M., O'Brien, S.P. and Streuli, M. (2000) The trio guanine nucleotide exchange factor is a RhoA target. Binding of RhoA to the trio immunoglobulin-like domain. J. Biol. Chem., 275, 36116-36123.
17. Jaiswal, M., Dvorsky, R. and Ahmadian, M.R. (2013) Deciphering the molecular and functional basis of Dbl family proteins: a novel systematic approach toward classification of selective activation of the Rho family proteins. J. Biol. Chem., 288, 4486-4500.
18. Blangy, A., Vignal, E., Schmidt, S., Debant, A., Gauthier-Rouvière, C. and Fort, P. (2000) TrioGEF1 controls Rac-and Cdc42-dependent cell structures through the direct activation of rhoG. J. Cell Sci., 113, 729-739.
19. Rossman, K.L., Der, C.J. and Sondek, J. (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol., 6, 167-180.
20. Choi, B.J., Imlach, W.L., Jiao, W., Wolfram, V., Wu, Y., Grbic, M., Cela, C., Baines, R.A., Nitabach, M.N. and McCabe, B.D. (2014) Miniature neurotransmission regulates Drosophila synaptic structural maturation. Neuron, 82, 618-634.
21. Ba, W., van der Raadt, J. and Nadif Kasri, N. (2013) Rho GTPase signaling at the synapse: implications for intellectual disability. Exp. Cell Res., 319, 2368-2374.
22. Newsome, T.P., Schmidt, S., Dietzl, G., Keleman, K., Asling, B., Debant, A. and Dickson, B.J. (2000) Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell, 101, 283-294.
23. Iyer, S.C., Wang, D., Iyer, E.P.R., Trunnell, S.A., Meduri, R., Shinwari, R., Sulkowski, M.J. and Cox, D.N. (2012) The RhoGEF trio functions in sculpting class specific dendrite morphogenesis in Drosophila sensory neurons. PLoS One, 7, e33634.
24. Shivalkar, M. and Giniger, E. (2012) Control of dendritic morphogenesis by Trio in Drosophila melanogaster. PLoS One, 7, e33737.
25. van Haren, J., Boudeau, J., Schmidt, S., Basu, S., Liu, Z., Lammers, D., Demmers, J., Benhari, J., Grosveld, F., Debant, A. et al. (2014) Dynamic microtubules catalyze formation of navigator-TRIO complexes to regulate neurite extension. Curr. Biol., 24, 1778-1785.
26. DeGeer, J., Boudeau, J., Schmidt, S., Bedford, F., Lamarche-Vane, N. and Debant, A. (2013) Tyrosine phosphorylation of the Rho guanine nucleotide exchange factor Trio regulates netrin-1/DCC-mediated cortical axon outgrowth. Mol. Cell Biol., 33, 739-751.
27. Briançon-Marjollet, A., Ghogha, A., Nawabi, H., Triki, I., Auziol, C., Fromont, S., Piché, C., Enslen, H., Chebli, K., Cloutier, J.-F. et al. (2008) Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell Biol., 28, 2314-2323.
28. Charrasse, S., Comunale, F., Fortier, M., Portales-Casamar, E., Debant, A. and Gauthier-Rouvière, C. (2007) M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion. Mol. Biol. Cell, 18, 1734-1743.
29. Schmidt, S. and Debant, A. (2014) Function and regulation of the Rho guanine nucleotide exchange factor Trio. Small GTPases, 5, 1-10.
30. O'Roak, B.J., Vives, L., Fu, W., Egertson, J.D., Stanaway, I.B., Phelps, I.G., Carvill, G., Kumar, A., Lee, C., Ankenman, K. et al. (2012) Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science, 338, 1619-1622.
31. Samocha, K.E., Robinson, E.B., Sanders, S.J., Stevens, C., Sabo, A., McGrath, L.M., Kosmicki, J.A., Rehnström, K., Mallick, S., Kirby, A. et al. (2014) A framework for the interpretation of de novo mutation in human disease. Nat. Genet., 46, 944-950.
32. Ma, X.-M., Huang, J.-P., Eipper, B.A. and Mains, R.E. (2005) Expression of Trio, a member of the Dbl family of Rho GEFs in the developing rat brain. J. Comp. Neurol., 482, 333-348.
33. McPherson, C.E., Eipper, B.A. and Mains, R.E. (2005) Multiple novel isoforms of Trio are expressed in the developing rat brain. Gene, 347, 125-135.
34. Zhou, D., Lambert, S., Malen, P.L., Carpenter, S., Boland, L.M. and Bennett, V. (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol., 143, 1295-1304.
35. Yan, Y., Eipper, B.A. and Mains, R.E. (2015) Kalirin-9 and Kalirin-12 play essential roles in dendritic outgrowth and branching. Cereb. Cortex 10, 3487-3501.
36. Bayés, A., Collins, M.O., Croning, M.D.R., van de Lagemaat, L.N., Choudhary, J.S. and Grant, S.G.N. (2012) Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins. PLoS One, 7, e46683.
37. Xie, Z., Srivastava, D.P., Photowala, H., Kai, L., Cahill, M.E., Woolfrey, K.M., Shum, C.Y., Surmeier, D.J. and Penzes, P. (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron, 56, 640-656.
38. Kiraly, D.D., Lemtiri-Chlieh, F., Levine, E.S., Mains, R.E. and Eipper, B.A. (2011) Kalirin binds the NR2B subunit of the NMDA receptor, altering its synaptic localization and function. J. Neurosci., 31, 12554-12565.
39. Kessels, H.W. and Malinow, R. (2009) Synaptic AMPA receptor plasticity and behavior. Neuron, 61, 340-350.
40. Nadif Kasri, N., Nakano-Kobayashi, A. and van Aelst, L. (2011) Rapid synthesis of the X-linked mental retardation protein OPHN1 mediates mGluR-dependent LTD through interaction with the endocytic machinery. Neuron, 72, 300-315.
41. Nadif Kasri, N., Nakano-Kobayashi, A., Malinow, R., Li, B. and van Aelst, L. (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev., 23, 1289-1302.
42. Sun, Y.-J., Nishikawa, K., Yuda, H., Wang, Y.-L., Osaka, H., Fukazawa, N., Naito, A., Kudo, Y., Wada, K. and Aoki, S. (2006) Solo/Trio8, a membrane-associated short isoform of Trio, modulates endosome dynamics and neurite elongation. Mol. Cell Biol., 26, 6923-6935.
43. Brown, T.C., Tran, I.C., Backos, D.S. and Esteban, J.A. (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron, 45, 81-94.
44. Lek, M. Exome Aggregation Consortium (2015) Analysis of Protein-Coding Genetic Variation in 60, 706 Humans doi:10.1101/030338
45. Hanse, E., Seth, H. and Riebe, I. (2013) AMPA-silent synapses in brain development and pathology. Nat. Rev. Neurosci. 14, 839-850.
46. Liao, D., Zhang, X., O'Brien, R., Ehlers, M.D. and Huganir, R.L. (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat. Neurosci., 2, 37-43.
47. Clement, J.P., Aceti, M., Creson, T.K., Ozkan, E.D., Shi, Y., Reish, N.J., Almonte, A.G., Miller, B.H., Wiltgen, B.J., Miller, C.A. et al. (2012) Pathogenic SYNGAP1 mutations impair cognitive development by disrupting maturation of dendritic spine synapses. Cell, 151, 709-723.
48. Olde Loohuis, N.F.M., Ba, W., Stoerchel, P.H., Kos, A., Jager, A., Schratt, G., Martens, G.J.M., van Bokhoven, H., Nadif Kasri, N. and Aschrafi, A. (2015) MicroRNA-137 controls AMPA-receptor-mediated transmission and mGluR-dependent LTD. Cell Rep., 11, 1876-1884.
49. Kasri, N.N., Govek, E.-E. and Aelst, L.V. (2008) Characterization of oligophrenin-1, a RhoGAP lost in patients affected with mental retardation: lentiviral injection in organotypic brain slice cultures. Methods Enzymol., 439, 255-266.
50. Carrodus, N.L., Teng, K.S.-L., Munro, K.M., Kennedy, M.J. and Gunnersen, J.M. (2014) Differential labeling of cell-surface and internalized proteins after antibody feeding of live cultured neurons. J.Vis. Exp.
51. Raynaud, F., Janossy, A., Dahl, J., Bertaso, F., Perroy, J., Varrault, A., Vidal, M., Worley, P.F., Boeckers, T.M., Bockaert, J. et al. (2013) Shank3-Rich2 interaction regulatesAMPAreceptor recycling and synaptic long-term potentiation. J. Neurosci., 33, 9699-9715.