Molecular networks implicated in speech-related disorders: FOXP2 regulates the SRPX2/uPAR complex

Human Molecular Genetics

Volumn 19, Issue 24, 2010, Pages 4848-4860

  Roll, Patrice ^a,b   Vernes, Sonja C ^c,f   Bruneau, Nadine ^a,b,d   Cillario, Jennifer ^a,b,d   Ponsole Lenfant, Magali ^a,b,d   Massacrier, Annick ^a,b,d   Rudolf, Gabrielle ^e   Khalife, Manal ^a,b,g   Hirsch, Edouard ^e   Fisher, Simon E ^c   Szepetowski, Pierre ^a,b,d  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^e UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^f RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^g CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; PLASMINOGEN ACTIVATOR; PROTEIN SRPX 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP2; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; BINDING SITE; BIOINFORMATICS; CHILD; CLINICAL ARTICLE; COMPUTER MODEL; DIMERIZATION; DOWN REGULATION; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; MALE; MICROGYRIA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SCHOOL CHILD; SPEECH DISORDER;

SYLVIA;

EID: 78649477258     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq415     Document Type: Article

References (43)

1. Fisher, S.E. (2009) On genes, speech, and language. N. Engl. J. Med., 353, 1655-1657.
2. Fisher, S.E. and Scharff, C. (2009) FOXP2 as a molecular window into speech and language. Trends Genet., 25, 166-177.
3. Lai, C.S., Fisher, S.E., Hurst, J.A., Vargha-Khadem, F. and Monaco, A.P. (2001) A forkhead-domain gene is mutated in a severe speech and language disorder. Nature, 413, 519-523.
4. MacDermot, K.D., Bonora, E., Sykes, N., Coupe, A.M., Lai, C.S., Vernes, S.C., Vargha-Khadem, F., McKenzie, F., Smith, R.L., Monaco, A.P. et al. (2005) Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am. J. Hum. Genet., 76, 1074-1080.
5. Zeesman, S., Nowaczyk, M.J., Teshima, I., Roberts, W., Cardy, J.O., Brian, J., Senman, L., Feuk, L., Osborne, L.R. and Scherer, S.W. (2006) Speech and language impairment and oromotor dyspraxia due to deletion of 7q31 that involves FOXP2. Am. J. Med. Genet., 140, 509-514.
6. Lehmann, O.J., Sowden, J.C., Carlsson, P., Jordan, T. and Bhattacharya, S.S. (2003) Fox's in development and disease. Trends Genet., 19, 339-344.
7. Shu, W., Cho, J.Y., Jiang, Y., Zhang, M., Weisz, D., Elder, G.A., Schmeidler, J., De Gasperi, R., Sosa, M.A., Rabidou, D. et al. (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc. Natl Acad. Sci. USA, 102, 9643-9648.
8. French, C.A., Groszer, M., Preece, C., Coupe, A.M., Rajewsky, K. and Fisher, S.E. (2007) Generation of mice with a conditional Foxp2 null allele. Genesis, 45, 440-446.
9. Haesler, S., Rochefort, C., Georgi, B., Licznerski, P., Osten, P. and Scharff, C. (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol., 5, e321.
10. Groszer, M., Keays, D.A., Deacon, R.M., de Bono, J.P., Prasad-Mulcare, S., Gaub, S., Baum, M.G., French, C.A., Nicod, J., Coventry, J.A. et al. (2008) Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr. Biol., 18, 354-362.
11. Miller, J.E., Spiteri, E., Condro, M.C., Dosumu-Johnson, R.T., Geschwind, D.H. and White, S.A. (2008) Birdsong decreases protein levels of FoxP2, a molecule required for human speech. J. Neurophysiol., 100, 2015-2025.
12. Enard, W., Gehre, S., Hammerschmidt, K., Hölter, M., Blass, T., Somel, M., Brückner, M.K., Schreiweis, C., Winter, C., Sohr, R. et al. (2009) A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell, 137, 961-971.
13. Spiteri, E., Konopka, G., Coppola, G., Bomar, J., Oldham, M., Ou, J., Vernes, S.C., Fisher, S.E., Ren, B., Geschwind, D.H. et al. (2007) Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am. J. Hum. Genet., 81, 1144-1157.
14. Vernes, S.C., Spiteri, E., Nicod, J., Groszer, M., Taylor, J.M., Davies, K.E., Geschwind, D.H. and Fisher, S.E. (2007) High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am. J. Hum. Genet., 81, 1232-1250.
15. Vernes, S.C., Newbury, D.F., Abrahams, B.S., Winchester, L., Nicod, J., Groszer, M., Alarcón, M., Oliver, P.L., Davies, K.E., Geschwind, D.H. et al. (2008) A functional genetic link between distinct developmental language disorders. N. Engl. J. Med., 359, 2337-2345.
16. Roll, P., Rudolf, G., Pereira, S., Royer, B., Scheffer, I.E., Massacrier, A., Valenti, M.P., Roeckel-Trevisiol, N., Jamali, S., Beclin, C. et al. (2006) SRPX2 mutations in disorders of language cortex and cognition. Hum. Mol. Genet., 15, 1195-1207.
17. Royer-Zemmour, B., Ponsole-Lenfant, M., Gara, H., Roll, P., Lévêque, C., Massacrier, A., Ferracci, G., Cillario, J., Robaglia-Schlupp, A., Vincentelli, R. et al. (2008) Epileptic and developmental disorders of the speech cortex: ligand/receptor interaction of wild-type and mutant SRPX2 with the plasminogen activator receptor uPAR. Hum. Mol. Genet., 17, 3617-3630.
18. Vernes, S.C., Nicod, J., Elahi, F.M., Coventry, J.A., Kenny, N., Coupe, A.M., Bird, L.E., Davies, K.E. and Fisher, S.E. (2006) Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum. Mol. Genet., 15, 3154-3167.
19. Rudolf, G., Valenti, M.P., Hirsch, E. and Szepetowski, P. (2009) From rolandic epilepsy to continuous spike-and-waves during sleep and Landau-Kleffner syndromes: insights into possible genetic factors. Epilepsia, 50 (Suppl. 7), 25-28.
20. Li, S., Weidenfeld, J. and Morrisey, E.E. (2004) Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions. Mol. Cell. Biol., 24, 809-822.
21. Alarcón, M., Abrahams, B.S., Stone, J.L., Duvall, J.A., Perederiy, J.V., Bomar, J.M., Sebat, J., Wigler, M., Martin, C.L., Ledbetter, D.H. et al. (2008) Linkage, association, and gene-expression analyses identify CNTNAP2 as an autism-susceptibility gene. Am. J. Hum. Genet., 82, 150-159.
22. Arking, D.E., Cutler, D.J., Brune, C.W., Teslovich, T.M., West, K., Ikeda, M., Rea, A., Guy, M., Lin, S., Cook, E.H. et al. (2008) A common genetic variant in the neurexin superfamily member CNTNAP2 increases familial risk of autism. Am. J. Hum. Genet., 82, 160-164.
23. Bakkaloglu, B., O'Roak, B.J., Louvi, A., Gupta, A.R., Abelson, J.F., Morgan, T.M., Chawarska, K., Klin, A., Ercan-Sencicek, A.G., Stillman, A.A. et al. (2008) Molecular cytogenetic analysis and resequencing of contactin associated protein-like 2 in autism spectrum disorders. Am. J. Hum. Genet., 82, 165-173.
24. Friedman, J.I., Vrijenhoek, T., Markx, S., Janssen, I.M., van der Vliet, W.A., Faas, B.H., Knoers, N.V., Cahn, W., Kahn, R.S., Edelmann, L. et al. (2008) CNTNAP2 gene dosage variation is associated with schizophrenia and epilepsy. Mol. Psychiatry, 13, 261-266.
25. Strauss, K.A., Puffenberger, E.G., Huentelman, M.J., Gottlieb, S., Dobrin, S.E., Parod, J.M., Stephan, D.A. and Morton, DH. (2006) Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2. N. Engl. J. Med., 354, 1370-1377.
26. Deonna, T.W., Roulet, E., Fontan, D. and Marcoz, JP. (1993) Speech and oromotor deficits of epileptic origin in benign partial epilepsy of childhood with rolandic spikes (BPERS). Relationship to the acquired aphasia-epilepsy syndrome. Neuropediatrics, 24, 83-87.
27. Staden, U., Isaacs, E., Boyd, S.G., Brandl, U. and Neville, B.G. (1998) Language dysfunction in children with rolandic epilepsy. Neuropediatrics, 29, 242-248.
28. Metz-Lutz, M.N., Kleitz, C., de Saint Martin, A., Massa, R., Hirsch, E. and Marescaux, C. (1999) Cognitive development in benign focal epilepsies of childhood. Dev. Neurosci., 21, 182-190.
29. Monjauze, C., Tuller, L., Hommet, C., Barthez, M.A. and Khomsi, A. (2005) Language in benign childhood epilepsy with centro-temporal spikes abbreviated form: rolandic epilepsy and language. Brain Lang., 92, 300-308.
30. Echenne, B., Cheminal, R., Rivier, F., Negre, C., Touchon, J. and Billiard, M. (1992) Epileptic electroencephalographic abnormalities and developmental dysphasias: a study of 32 patients. Brain Dev., 14, 216-225.
31. Durand, C.M., Betancur, C., Boeckers, T.M., Bockmann, J., Chaste, P., Fauchereau, F., Nygren, G., Rastam, M., Gillberg, I.C., Anckarsäter, H. et al. (2007) Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet., 39, 25-27.
32. Liégeois, F., Baldeweg, T., Connelly, A., Gadian, D.G., Mishkin, M. and Vargha-Khadem, F. (2003) Language fMRI abnormalities associated with FOXP2 gene mutation. Nat. Neurosci., 6, 1230-1237.
33. Abrahams, B.S., Tentler, D., Perederiy, J.V., Oldham, M.C., Coppola, G. and Geschwind, D.H. (2007) Genome-wide analyses of human perisylvian cerebral cortical patterning. Proc. Natl Acad. Sci. USA, 104, 17849-17854.
34. Johnson, M.B., Kawasawa, Y.I., Mason, C.E., Krsnik, Z., Coppola, G., Bogdanovic, D., Geschwind, D.H., Mane, S.M., State, M.W. and Sestan, N. (2009) Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron, 62, 494-509.
35. Enard, W., Przeworski, M., Fisher, S.E., Lai, C.S., Wiebe, V., Kitano, T., Monaco, A.P. and Pääbo, S. (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature, 418, 869-872.
36. Konopka, G., Bomar, J.M., Winden, K., Coppola, G., Jonsson, Z.O., Gao, F., Peng, S., Preuss, T.M., Wohlschlegel, J.A. and Geschwind, D.H. (2009) Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature, 462, 213-217.
37. Royer, B., Soares, D.C., Barlow, P.N., Bontrop, R.E., Roll, P., Robaglia-Schlupp, A., Blancher, A., Levasseur, A., Cau, P., Pontarotti, P. et al. (2007) Molecular evolution of the human SRPX2 gene that causes brain disorders of the rolandic and Sylvian speech areas. BMC Genet., 8, 72.
38. Wang, H., Yang, L., Jamaluddin, M.S. and Boyd, D.D. (2004) The Kruppel-like KLF4 transcription factor, a novel regulator of urokinase receptor expression, drives synthesis of this binding site in colonic crypt luminal surface epithelial cells. J. Biol. Chem., 279, 22674-22683.
39. Büchler, P., Reber, H.A., Tomlinson, J.S., Hankinson, O., Kallifatidis, G., Friess, H., Herr, I. and Hines, O.J. (2009) Transcriptional regulation of urokinase-type plasminogen activator receptor by hypoxia-inducible factor 1 is crucial for invasion of pancreatic and liver cancer. Neoplasia, 11, 196-206.
40. Kurosawa, H., Goi, K., Inukai, T., Inaba, T., Chang, K.S., Shinjyo, T., Rakestraw, K.M., Naeve, C.W. and Look, A.T. (1999) Two candidate downstream target genes for E2A-HLF. Blood, 93, 321-332.
41. Fledderus, J.O., Boon, R.A., Volger, O.L., Hurttila, H., Ylä-Herttuala, S., Pannekoek, H., Levonen, A.L. and Horrevoets, A.J. (2008) KLF2 primes the antioxidant transcription factor Nrf2 for activation in endothelial cells. Arterioscler. Thromb. Vasc. Biol., 28, 1339-1346.
42. Stothard, P. (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques, 28, 1102-1114.
43. Takahashi, M., Matsuda, F., Margetic, N. and Lathrop, M. (2003) Automated identification of single nucleotide polymorphisms from sequencing data. J. Bioinform. Comput. Biol., 1, 253-265.