Intragenic rearrangements in X-linked intellectual deficiency: Results of a-CGH in a series of 54 patients and identification of TRPC5 and KLHL15 as potential XLID genes

American Journal of Medical Genetics, Part A

Volumn 164, Issue 8, 2014, Pages 1991-1997

  Mignon Ravix, Cécile ^a,b   Cacciagli, Pierre ^a,b,c   Choucair, Nancy ^a,b,d   Popovici, Cornel ^c   Missirian, Chantal ^c   Milh, Mathieu ^a,b,c   Mégarbané, André ^a,b,d   Busa, Tiffany ^c   Julia, Sophie ^e   Girard, Nadine ^b,c   Badens, Catherine ^a,b,c   Sigaudy, Sabine ^c   Philip, Nicole ^a,b,c   Villard, Laurent ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c TIMONE HOSPITAL   (France)

^d SAINT JOSEPH UNIVERSITY   (Lebanon)

^e CHU PURPAN   (France)

Author keywords

Array CGH; KLHL15; TRPC5; X linked intellectual disability

Indexed keywords

ARTICLE; AUTISM; CELL GROWTH; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CORTICAL DYSPLASIA; DENDRITIC CELL; EPILEPSY; EXON; FAMILY HISTORY; FMRI GENE; GENE; GENE DUPLICATION; GENE IDENTIFICATION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ANALYSIS; GENETIC VARIABILITY; HUMAN; IL1RAPL1 GENE; INHERITANCE; INTELLECTUAL IMPAIRMENT; KLHL15 GENE; MAJOR CLINICAL STUDY; MALE; MAP7D3 GENE; MECP2 GENE; MISSENSE MUTATION; OPHN1 GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TRPC5 GENE; X CHROMOSOME INACTIVATION; X CHROMOSOME LINKED DISORDER; X LINKED INTELLECTUAL DEFICIENCY; XLID GENE; CHROMOSOME MAP; COPY NUMBER VARIATION; GENE DELETION; GENE LOCUS; GENE TRANSLOCATION; GENETIC ASSOCIATION; GENETICS; INTELLECTUAL DISABILITY; PRESCHOOL CHILD; X CHROMOSOMAL INHERITANCE; X CHROMOSOME;

ACTIN BINDING PROTEIN; KLHL15 PROTEIN, HUMAN; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC5 PROTEIN, HUMAN;

CHILD, PRESCHOOL; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, X; COMPARATIVE GENOMIC HYBRIDIZATION; DNA COPY NUMBER VARIATIONS; GENE DELETION; GENES, X-LINKED; GENETIC LOCI; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INTELLECTUAL DISABILITY; MALE; MICROFILAMENT PROTEINS; TRANSLOCATION, GENETIC; TRPC CATION CHANNELS; X CHROMOSOME INACTIVATION;

EID: 84904394913     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.36602     Document Type: Article

References (42)

1. Alesi V, Bertoli M, Barrano G, Torres B, Pusceddu S, Pastorini M, Perria C, Nardone AM, Novelli A, Serra G. 2012. 335.4kb microduplication in chromosome band Xp11.2p11.3 associated with developmental delay, growth retardation, autistic disorder and dysmorphic features. Gene 505:384-387.
2. Al-Owain M, Kaya N, Al-Zaidan H, Al-Hashmi N, Al-Bakheet A, Al-Muhaizea M, Chedrawi A, Basran RK, Milunsky A. 2011. Novel intragenic deletion in OPHN1 in a family causing XLMR with cerebellar hypoplasia and distinctive facial appearance. Clin Genet 79:363-370.
3. Barone C, Bianca S, Luciano D, Di Benedetto D, Vinci M, Fichera M. 2013. Intragenic IL1RAPL1 deletion in a male patient with intellectual disability, mild dysmorphic signs, deafness, and behavioral problems. Am J Med Genet Part A 161A:1381-1385.
4. Behnecke A, Hinderhofer K, Bartsch O, Nümann A, Ipach ML, Damatova N, Haaf T, Dufke A, Riess O, Moog U. 2011. Intragenic deletions of IL1RAP L1: Report of two cases and review of the literature. Am J Med Genet Part A 155A:372-379.
5. Bergmann C, Zerres K, Senderek J, RudnikSchoneborn S, Eggermann T, Haüsler M, Mull M, Ramaekers VT. 2003. Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cerebellar hypoplasia. Brain 126:1537-1544.
6. Carrié A, Jun L, Bienvenu T, Vinet MC, McDonell N, Couvert P, Zemni R, Cardona A, Van Buggenhout G, Frints S, Hamel B, Moraine C, Ropers HH, Strom T, Howell GR, Whittaker A, Ross MT, Kahn A, Fryns JP, Beldjord C, Marynen P, Chelly J. 1999. A new member of the IL-1 receptor family highly expressed in hippocampus and involved in X-linked mental retardation. Nat Genet 23:25-31.
7. Chiurazzi P, Schwartz CE, Getz J, Neri G. 2008. XLMR genes: Update 2007. Eur J Hum Genet 16:422-434.
8. des Portes V, Beldjord C, Chelly J, Hamel B, Kremer H, Smits A, van Bokhoven H, Ropers HH, Claes S, Fryns JP, Ronce N, Gendrot C, Toutain A, Raynaud M, Moraine C. 1999. X-linked nonspecific mental retardation (MRX) linkage studies in 25 unrelated families: The European XLMR consortium. Am J Med Genet 85:263-265.
9. Freichel M, Vennekens R, Olausson J, Stolz S, Philipp SE, Weissgerber P, Flockerzi V. 2005. Functional role of TRPC proteins in native systems: Implications from knockout and knock-down studies. J Physiol 567:59-66.
10. Froyen G, Van Esch H, Bauters M, Hollanders K, Frints SG, Vermeesch JR, Devriendt K, Fryns JP, Marynen P. 2007. Detection of genomic copy number changes in patients with idiopathic mental retardation by High-resolution X-array-CGH: Important role for increased gene dosage of XLMR genes. Hum Mutat 28:1034-1042.
11. Gecz J, Shoubridge C, Corbett M. 2009. The genetic landscape of intellectual disability arising from chromosome X. Trends Genet 25:308-316.
12. Gillardon F. 2009. Leucine-rich repeat kinase 2 phosphorylates brain tubulin-beta isoforms and modulates microtubule stability-A point of convergence in parkinsonian neurodegeneration? J Neurochem 110:1514-1522.
13. Gu XX, Decorte R, Marynen P, Fryns JP, Cassiman JJ, Raeymaekers P. 1996. Localisation of a new gene for non-specific mental retardation to Xq22-q26 (MRX35). J Med Genet 33:52-55.
14. He Z, Jia C, Feng S, Zhou K, Tai Y, Bai X, Wang Y. 2012. TRPC5 channel is the mediator of neurotrophin-3 in regulating dendritic growth via CaMKIIα in rat hippocampal neurons. J Neurosci 32:9383-9395.
15. Heo DK, Chung WY, Park HW, Yuan JP, Lee MG, Kim JY. 2012. Opposite regulatory effects of TRPC1 and TRPC5 on neurite outgrowth in PC12 cells. Cell Signal 24:899-906.
16. Isrie M, foryen G, Devirendt K, de Ravel T, Fryns JP, Vermeesch JR, Van Esch H. 2012. Sporadic patients with intellectual disability: Contribution of X-chromosome copy number variants. Eur J Med Genet 55:577-585.
17. Kaczmarek JS, Riccio A, Clapham DE. 2012. Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc Natl Acad Sci USA 109:7888-7892.
18. Lubs HA, Stevenson RE, Schwartz CE. 2012. Fragile X and X-linked intellectual disability: Four decades of discovery. Am J Hum Genet 90:579-590.
19. Lugtenberg D, Veltman JA, van Brokhoven H. 2007. High-resolution genomic microarrays for X-linked mental retardation. Genet Med 9:560-565.
20. Madrigal I, Rodriguez-Revenga L, Armengol L, Gonzalez E, Rodriguez B, Badenas C, Sanchez A, Martinez F, Guitart M, Fernandez I, Arranz JA, Tejada M, Perez-jurado LA, Estivill X, Mila M. 2007. X-chromosome tiling path array of copy number variants in patients with chromosome X-linked mental retardation. BMC Genomics 8:443.
21. Madrigal I, Rodríguez-Revenga L, Badenas C, Sánchez A, Milà M. 2008. Deletion of the OPHN1 gene detected by aCGH. J Intellect Disabil Res 52:190-194.
22. Nawara M, Klapecki J, Borg K, Jurek M, Moreno S, Tryfon J, Bal J, Chelly J, Mazurczak T. 2008. Novel mutation of IL1RAPL1 gene in a nonspecific X linked mental retardation (MRX) family. Am J Med Genet Part A 146A:3167-3172.
23. Oberg EA, Nifoussi SK, Gingras AC, Strack S. 2012. Selective proteasomal degradation of the B'β subunit of protein phosphatase 2A by the E3 ubiquitin ligase adaptor Kelch-like 15. J Biol Chem 287:43378-43389.
24. Phelan KD, Shwe UT, Abramowitz J, Wu H, Rhee SW, Howell MD, Gottschall PE, Freichel M, Flockerzi V, Birnbaumer L, Zheng F. 2013. Canonical transient receptor channel 5 (TRPC5) and TRPC1/4 contribute to seizure and excitotoxicity by distinct cellular mechanisms. Mol Pharmacol 83:429-438.
25. Piton A, Michaud JL, Peng H, Aradhya S, Gauthier J, Mottron L, Champagne N, Lafrenière RG, Hamdan FF, S2D Team, Joober R, Fombonne E, Marineau C, Cossette P, Dubé MP, Haghighi P, Drapeau P, Barker PA, Carbonetto S, Rouleau GA, 2011. Mutations in the calcium-related gene IL1RAPL1 are associated with autism. Mol Psychiatry 16:867-880.
26. Piton A, Redin C, Mandel JL. 2013. XLID-Causing mutations and associated genes challenged in light of data from large-scale human exome sequencing. Am J Hum Genet 93:368-383.
27. Poulain FE, Sobel A. 2010. The microtubule network and neuronal morphogenesis: Dynamic and coordinated orchestration through multiple players. Mol Cell Neurosci 43:15-32.
28. Puram SV, Riccio A, Koirala S, Ikeuchi Y, Kim AH, Corfas G, Bonni A. 2011. A TRPC5-regulated calcium signaling pathway controls dendrite patterning in the mammalian brain. Genes Dev 25:2659-2673.
29. Riccio A, Li Y, Moon J, Kim KS, Smith KS, Rudolph U, Gapon S, Yao GL, Tsvetkov E, Rodig SJ, Van't Veer A, Meloni EG, Carlezon WA, Bolshakov VY, Clapham DE. 2009. Essential role for TRPC5 in amygdala function and fear-related behavior. Cell 137:761-772.
30. Rio M, Malan V, Boissel S, Toutain A, Royer G, Gobin S, Morichon-Delvallez N, Turleau C, Bonnefont JP, Munnich A, Vekemans M, Colleaux L. 2010. Familial interstitial Xq27.3q28 duplication encompassing the FMR1 gene but not MECP2 gene causes a new syndromic mental retardation condition. Eur J Hum Genet 18:285-290.
31. Ropers HH. 2010. Genetics of early onset cognitive impairment. Annu Rev Genomics Hum Genet 11:161-187.
32. Ropers HH, Hamel BC. 2005. X-linked mental retardation. Nat Rev Genet 6:46-57.
33. Rovelet-Lecrux A, Lecourtois M, Thomas-Anterion C, Le Ber I, Brice A, Frebourg T, Hannequin D, Campion D. 2009. Partial deletion of the MAPT gene: A novel mechanism of FTDP-17. Hum Mutat 30:E591-E602.
34. Santos-Rboucas CB, Belet S, Guedes de Almeida L, Ribeiro MG, Medina-Acosta E, Bahia PR, Alves da Silva AF, Lima Dos Santos F, Borges de Lacerda GC, Pimentel MM, Froyen G. 2014. A novel in-frame deletion affecting the BAR domain of OPHN1 in a family with intellectual disability and hippocampal alterations. Eur J Hum Genet 22:644-651.
35. Shin HY, Hong YH, Jang SS, Chae HG, Paek SL, Moon HE, Kim DG, Kim J, Paek SH, Kim SJ. 2010. A role of canonical transient receptor potential 5 channel in neuronal differentiation from A2B5 neural progenitor cells. PLoS ONE 5:e10359.
36. 2+ entry channel. Genomics 60:330-340.
37. Sun X, Shi X, Liu M, Li D, Zhang L, Liu X, Zhou J. 2011. Mdp3 is a novel microtubule-binding protein that regulates microtubule assembly and stability. Cell Cycle 10:3929-3937.
38. Tarpey PS, Smith R, Pleasance E, Whibley A, Edkins S, Hardy C, O'Meara S, Latimer C, Dicks E, Menzies A, Stephens P, Blow M, Greenman C, Xue Y, Tyler-Smith C, Thompson D, Gray K, Andrews J, Barthorpe S, Buck G, Cole J, Dunmore R, Jones D, Maddison M, Mironenko T, Turner R, Turrell K, Varian J, West S, Widaa S, Wray P, Teague J, Butler A, Jenkinson A, Jia M, Richardson D, Shepherd R, Wooster R, Tejada MI, Martinez F, Carvill G, Goliath R, de Brouwer AP, van Bokhoven H, Van Esch H, Chelly J, Raynaud M, Ropers HH, Abidi FE, Srivastava AK, Cox J, Luo Y, Mallya U, Moon J, Parnau J, Mohammed S, Tolmie JL, Shoubridge C, Corbett M, Gardner A, Haan E, Rujirabanjerd S, Shaw M, Vandeleur L, Fullston T, Easton DF, Boyle J, Partington M, Hackett A, Field M, Skinner C, Stevenson RE, Bobrow M, Turner G, Schwartz CE, Gecz J, Raymond FL, Futreal PA, Stratton MR. 2009. A systematic, large-scale reseuqencing screen of X-chromosome coding exons in mental retardation. Nat Genet 41:535-543.
39. Van Esch H, Bauters M, Ignatius J, Jansen M, Raynaud M, Hollanders K, Lugtenberg D, Bienvenu T, Jensen LR, Gecz J, Moraine C, Marynen P, Fryns JP, Froyen G. 2005. Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Am J Hum Genet 77:442-453.
40. Villard L, Levy N, Xiang F, Kpebe A, Labelle V, Chevillard C, Zhang Z, Schwartz CE, Tardieu M, Chelly J, Anvret M, Fontes M. 2001. Segregation of a totally skewed pattern of X chromosome inactivation in four familial cases of Rett syndrome without MECP2 mutation: Implications for the disease. J Med Genet 38:435-442.
41. Xie R, Nguyen S, McKeehan K, Wang F, McKeehan WL, Liu L. 2011. Microtubule-associated protein 1S (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation. J Biol Chem 286:10367-10377.
42. Zanni G, Saillour Y, Nagara M, Billuart P, Castelnau L, Moraine C, Faivre L, Bertini E, Durr A, Guichet A, Rodriguez D, des Portes V, Beldjord C, Chelly J. 2005. Oligophrenin 1 mutations frequently cause X-linked mental retardation with cerebellar hypoplasia. Neurology 65:1364-1369.