Monogenic causes of x-linked mental retardation

Nature Reviews Genetics

Volumn 2, Issue 9, 2001, Pages 669-680

  Chelly, Jamel ^a   Mandel, Jean Louis ^b  

^a CHU Cochin ^*  (France)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME MAP; GENETIC LINKAGE; GENETICS; HUMAN; MALE; MENTAL DEFICIENCY; REVIEW; X CHROMOSOME;

CHROMOSOME MAPPING; HUMANS; LINKAGE (GENETICS); MALE; MENTAL RETARDATION; X CHROMOSOME;

EID: 0035464960     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35088558     Document Type: Article

References (113)

1. Moser, H. W., Ramey, C. T. & Leonard, C. O. in Principles and Practice of Medical Genetics Vol. I (eds Emery, A. E. H. & Rimoin, D. L.) 495-511 (Churchill Livingstone, Edinburgh, 1990).
2. Stevenson, R. E., Schwartz, C. E. & Schroer, R. J. X-Linked Mental Retardation (Oxford Univ. Press, 2000). An excellent and timely book that gives an extensive overview of epidemiological studies and clinical descriptions of all XLMR syndromes.
3. McLaren, J. & Bryson, S. E. Review of recent epidemiological studies of mental retardation: prevalence, associated disorders, and etiology. Am. J. Ment. Retard. 92, 243-254 (1987).
4. Shaffer, L. G., Ledbetter, D. H. & Lupski, J. R. in The Metabolic and Molecular Bases of Inherited Disease Vol. I (eds Scriver, C. R., Beaudet, A. L. Sly, W. S. & Valle, D.) 1291-1326 (McGraw-Hill, New York, 2001).
5. Donnai, D. & Karmiloff-Smith, A. Williams syndrome: from genotype through to the cognitive phenotype. Am. J. Med. Genet. 97, 164-171 (2000).
6. Knight, S. J. et al. Subtle chromosomal rearrangements in children with unexplained mental retardation. Lancet 354, 1676-1681 (1999).
7. Hagerman, R. J. & Cronister, A. Fragile X Syndrome: Diagnosis, Treatment and Research (Johns Hopkins Univ. Press, Baltimore, 1996).
8. Imbert, G., Feng, Y., Nelson, D., Warren, S. T. & Mandel, J.-L. in Genetic Instabilities and Hereditary Neurological Diseases (eds Warren, S. T. & Wells, R. D.) 27-53 (Academic, San Diego, 1998).
9. Chiurazzi, P., Hamel, B. C. & Neri, G. XLMR genes: update 2000. Eur. J. Hum. Genet. 9, 71-61 (2001). The complete list of XLMR loci, which is regularly updated on the Web (see link to XLMR Genes Update web site).
10. Bardoni, B., Mandel, J. L. & Fisch, G. S. FMR1 gene and fragile X syndrome. Am. J. Med. Genet. 97, 153-163 (2000).
11. Gibbons, R. J., Picketts, D. J., Villard, L. & Higgs, D. R. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with α-thalassemia (ATR-X syndrome). Cell 80, 837-845 (1995). This paper reports the Identification of the ATRX syndrome gene, and the following seven references outline the phenotypic and mutation diversity of this syndrome.
12. Gibbons, R. J. & Higgs, D. R. Molecular-clinical spectrum of the ATR-X syndrome. Am. J. Med. Genet. 97, 204-212 (2000).
13. Gibbons, R. J. et al. Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nature Genet. 17, 146-148 (1997).
14. Villard, L. et al. XNP mutation in a large family with Juberg-Marsidi syndrome. Nature Genet. 12, 359-360 (1996).
15. Villard, L., Fontes, M., Ades, L. C. & Gecz, J. Identification of a mutation in the XNP/ATR-X gene in a family reported as Smith-Fineman-Myers syndrome. Am. J. Med. Genet. 91, 83-85 (2000).
16. Stevenson, R. E. Splitting and lumping in the nosology of XLMR. Am. J. Med. Genet. 97, 174-182 (2000).
17. Guerrini, R. et al. A nonsense mutation of the ATRX gene causing mild mental retardation and epilepsy. Ann. Neurol. 47, 117-121 (2000).
18. Lossi, A. M. et al. Mutation of the XNP/ATR-X gene in a family with severe mental retardation, spastic paraplegia and skewed pattern of X inactivation: demonstration that the mutation is involved in the inactivation bias. Am. J. Hum. Genet. 65, 558-562 (1999).
19. McDowell, T. L. et al. Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl Acad. Sci. USA 96, 13983-13988 (1999).
20. Le Douarin, B. et al. A possible involvement of TIF1α and TIF1β in the epigenetic control of transcription by nuclear receptors. EMBO J. 15, 6701-6715 (1996).
21. Cardoso, C. et al. Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum. Mol. Genet. 7, 679-684 (1998).
22. Berube, N. G., Smeenk, C. A. & Picketts, D. J. Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum. Mol. Genet. 9, 539-547 (2000).
23. Gibbons, R. J. et al. Mutations in ATPX, encoding an SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nature Genet. 24, 368-371 (2000).
24. Trivier, E. et al. Mutations in the kinase Rsk-2 associated with Coffin-Lowry syndrome. Nature 384, 567-570 (1996). This paper reports the identification of the Coffin-Lowry gene, and reference 27 extends the associated phenotypes to mild, nonspecific retardation.
25. Yntema, H. G. et al. A novel ribosomal S6-kinase (RSK4; RPS6KA6) is commonly deleted in patients with complex X-linked mental retardation. Genomes 62, 332-343 (1999).
26. Delaunoy, J. et al. Mutations in the X-linked RSK2 gene (RPS6KA3) in patients with Coffin-Lowry syndrome. Hum. Mutat. 17, 103-116 (2001).
27. Merienne, K. et al. A missense mutation in RPS6KA3 (RSK2) responsible for non-specific mental retardation. Nature Genet. 22, 13-14 (1999).
28. De Cesare, D., Jacquot, S., Hanauer, A. & Sassone-Corsi, P. Rsk-2 activity is necessary for epidermal growth factor-induced phosphorylation of CREB protein and transcription of c-fos gene. Proc. Natl Acad. Sci. USA 95, 12202-12207 (1998).
29. Sassone-Corsi, P. et al. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 285, 886-891 (1999).
30. Merienne, K., Pannetier, S., Harel-Bellan, A. & Sassone-Corsi, P. The mitogen-regulated RSK2-CBP interaction controls their kinase and acetylase activities. Mol. Cell. Biol. (in the press).
31. Sirianni, N., Naidu, S., Pereira, J., Pillotto, R. F. & Hoffman, E. P. Rett syndrome: confirmation of X-linked dominant inheritance, and localization of the gene to Xq28. Am. J. Hum. Genet. 63, 1552-1558 (1998).
32. Amir, R. E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nature Genet. 23, 185-188 (1999). This landmark paper solved the long-standing enigma of the genetic basis of Rett syndrome, with the identification of MECP2 mutations in Rett patients, and posed new questions about the role of MECP2 in neuron maintenance.
33. Amir, R. & Zoghbi, H. Rett syndrome: methyl-CpG-binding protein 2 mutations and phenotype-genotype correlations. Am. J. Med. Genet. Sem. Med. Genet. 97, 147-152 (2000).
34. Bourdon, V. et al. A detailed analysis of the MECP2 gene: prevalence of recurrent mutations and gross DNA rearrangements in Rett syndrome patients. Hum. Genet. 108, 43-50 (2001).
35. Laccone, F., Huppke, P., Hanefeld, F. & Meins, M. Mutation spectrum in patients with Rett syndrome in the German population: evidence of hot spot regions. Hum. Mutat. 17, 183-190 (2001).
36. Meloni, I. et al. A mutation in the Rett syndrome gene, MECP2, causes X-linked mental retardation and progressive spasticity in males. Am. J. Hum. Genet. 67, 982-985 (2000).
37. Orrico, A. et al. MECP2 mutation in male patients with non-specific X-linked mental retardation. FEBS Lett. 481, 285-288 (2000).
38. Couvert, P. et al. MECP2 is highly mutated in X-linked mental retardation. Hum. Mol. Genet 10, 941-946 (2001). This paper indicates that MECP2 mutations might be the second most frequent known cause of XLMR in males.
39. Robertson, K. D. & Wolffe, A. P. DNA methylation in health and disease. Nature Rev. Genet. 1, 11-19 (2000).
40. Chen, R. Z., Akbarian, S., Tudor, M. & Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nature Genet. 27, 327-331 (2001). This and the following reference describe the very interesting phenotype of the Mecp2-knockout mouse, which models some aspects of Rett syndrome.
41. Guy, J., Hendrich, B., Holmes, M., Martin, J. E. & Bird, A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nature Genet. 27, 322-326 (2001).
42. des Portes, V. et al. X-linked nonspecific mental retardation (MRX) linkage studies in 25 unrelated families: the European XLMR consortium. Am. J. Med. Genet. 85, 263-265 (1999).
43. Gu, Y., Shen, Y., Gibbs, R. A. & Nelson, D. L. Identification of FMR2, a novel gene associated with the FRAXE CCG repeat and CpG island. Nature Genet. 13, 109-113 (1996).
44. Gecz, J., Gedeon, A. K., Sutherland, G. R. & Mulley, J. C. Identification of the gene FMR2, associated with FRAXE mental retardation. Nature Genet. 13, 105-108 (1996).
45. Knight, S. J. et al. Triplet repeat expansion at the FRAXE locus and X-linked mild mental handicap. Am. J. Hum. Genet. 55, 81-86 (1994).
46. Youings, S. A. et al. FRAXA and FRAXE: the results of a five year survey. J. Med. Genet. 37, 415-421 (2000).
47. Gecz, J., Bielby, S., Sutherland, G. R. & Mulley, J. C. Gene structure and subcellular localization of FMR2, a member of a new family of putative transcription activators. Genomics 44, 201-213 (1997).
48. Miller, W. J., Skinner, J. A., Foss, G. S. & Davies, K. E. Localization of the fragile X mental retardation 2 (FMR2) protein in mammalian brain. Eur. J. Neurosci. 12, 381-384 (2000).
49. Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nature Rev. Mol. Cell. Biol. 2, 107-117 (2001).
50. Geppert, M. & Sudhof, T. C. RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu. Rev. Neurosci. 21, 75-95 (1998).
51. D'Adamo, P. et al. Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nature Genet. 19, 134-139 (1998).
52. Bienvenu, T. et al. Non-specific X-linked semidominant mental retardation by mutations in a Rab GDP-dissociation inhibitor. Hum. Mol. Genet. 7, 1311-1315 (1998).
53. Ishizaki, H. et al. Role of rab GDP dissociation inhibitor alpha in regulating plasticity of hippocampal neurotransmission. Proc. Natl Acad. Sci. USA 97, 11587-11592 (2000).
54. Geppert, M. et al. The role of Rab3A in neurotransmitter release. Nature 369, 493-497 (1994).
55. Billuart, P. et al. Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392, 923-926 (1998).
56. Dickson, B. J. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103-110 (2001).
57. Bagrodia, S., Derijard, B., Davis, R. J. & Cerione, R. A. Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270, 27995-27998 (1995).
58. Manser, E. et al. Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) family. J. Biol. Chem. 270, 25070-25078 (1995).
59. Allen, K. M. et al. PAK3 mutation in nonsyndromic X-linked mental retardation. Nature Genet. 20, 25-30 (1998).
60. Bienvenu, T. et al. Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am. J. Med. Genet. 93, 294-298 (2000).
61. Kutsche, K. et al. Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nature Genet. 26, 247-250 (2000).
62. Manser, E. et al. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192 (1998).
63. Takagi, S. et al. Identification of a highly specific surface marker of T-cell acute lymphoblastic leukemia and neuroblastoma as a new member of the transmembrane 4 superfamily. Int. J. Cancer 61, 706-715 (1995).
64. Zemni, R. et al. A new gene involved in X-linked mental retardation identified by analysis of an X;2 balanced translocation. Nature Genet. 24, 167-170 (2000).
65. Maecker, H. T., Todd, S. C. & Levy, S. The tetraspanin superfamily: molecular facilitators. FASEB J. 11, 428-442 (1997).
66. Kopczynski, C. C., Davis, G. W. & Goodman, C. S. A neural tetraspanin, encoded by late bloomer, that facilitates synapse formation. Science 271, 1867-1870 (1996).
67. Rohrbough, J., Grotewiel, M. S., Davis, R. L. & Broadie, K. Integrin-mediated regulation of synaptic morphology, transmission, and plasticity. J. Neurosci. 20, 6868-6878 (2000).
68. Carrié, A. et al. A new member of the IL-1 receptor family highly expressed in hippocampus and involved in X-linked mental retardation. Nature Genet. 23, 25-31 (1999).
69. Brunner, H. G. et al. X-linked borderline mental retardation with prominent behavioral disturbance: phenotype, genetic localization, and evidence for disturbed monoamine metabolism. Am. J. Hum. Genet. 52, 1032-1039 (1993).
70. Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H. & Van Oost, B. A. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262, 578-580 (1993).
71. Cases, O. et al. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268, 1763-1766 (1995).
72. Ibanez, A., de Castro, I. P., Fernandez-Piqueras, J., Blanco, C. & Saiz-Ruiz, J. Pathological gambling and DNA polymorphic markers at MAO-A and MAO-B genes. Mol. Psychiatry 5, 105-109 (2000).
73. Schmidt, L. G. et al. Different allele distribution of a regulatory MAOA gene promoter polymorphism in antisocial and anxious-depressive alcoholics. J. Neural Transm. 107, 681-689 (2000).
74. Schuback, D. E. et al. Screen for MAOA mutations in target human groups. Am. J. Med. Genet. 88, 25-28 (1999).
75. Pattison, L. et al. A fifth locus for primary autosomal recessive microcephaly maps to chromosome 1q31. Am. J. Hum. Genet. 67, 1578-1580 (2000).
76. Wirth, J. et al. Systematic characterisation of disease associated balanced chromosome rearrangements by FISH: cytogenetically and genetically anchored YACs identify microdeletions and candidate regions for mental retardation genes. J. Med. Genet. 36, 271-278 (1999).
77. Cheadle, J. P. et al. Long-read sequence analysis of the MECP2 gene in Rett syndrome patients: correlation of disease severity with mutation type and location. Hum. Mol. Genet. 9, 1119-1129 (2000).
78. Wan, M. et al. Rett syndrome and beyond: recurrent spontaneous and familial MECP2 mutations at CpG hot spots. Am. J. Hum. Genet. 65, 1520-1529.
79. Willemsen, R. et al. Noninvasive test for fragile X syndrome, using hair root analysis. Am. J. Hum. Genet. 65, 98-103 (1999).
80. Merienne, K. et al. Rapid immunoblot and kinase assay tests for a syndromal form of X linked mental retardation: Coffin-Lowry syndrome. J. Med. Genet. 35, 890-894 (1998).
81. Gronskov, K., Hallberg, A. & Brondum-Nielsen, K. Mutational analysis of the FMR1 gene in 118 mentally retarded males suspected of fragile X syndrome: absence of prevalent mutations. Hum. Genet. 102, 440-445 (1998).
82. Chelly, J. Breakthroughs in molecular and cellular mechanisms underlying X-linked mental retardation. Hum. Mol. Genet. 8, 1833-1838 (1999).
83. Luo, L. Rho GTPases in neuronal morphogenesis. Nature Rev. Neurosci. 1, 173-180 (2000).
84. Comery, T. A. et al. Abnormal dendritic spines in fragile X knock-out mice: maturation and pruning deficits. Proc. Natl Acad. Sci. USA 94, 5401-5404 (1997).
85. Hacia, J. G. & Collins, F. S. Mutational analysis using oligonucleotide microarrays. J. Med. Genet. 36, 730-736 (1999).
86. Moch, H. et al. High-throughput tissue microarray analysis to evaluate genes uncovered by cDNA microarray screening in renal cell carcinoma. Am. J. Pathol. 154, 981-986 (1999).
87. Burgemeister, B. B., Hollander, Blum, L. & Lorge, I. Manual for the Use of the Columbia Mental Maturity Scale (The Psychological corporation, New York, 1972).
88. Wechsler, D. Wechsler Adult Intelligence Scale - Revised (WAIS-R) Manual (The Psychological Corporation, New York, 1981).
89. Plomin, R. Genetics and general cognitive ability. Nature 401, C25-C29 (1999).
90. Vogel, F. & Motulsky, A. G. (eds) Human Genetics. Problems and Approaches 3rd edn (Springer, Berlin/Heidelberg, 1996).
91. Gecz, J. FMR3 is a novel gene associated with FRAXE CpG island and transcriptionally silent in FRAXE full mutations. J. Med. Genet. 37, 782-784 (2000).
92. Giancotti, F. G. Integrin signaling: specificity and control of cell survival and cell cycle progression. Curr. Opin. Cell Biol. 9, 691-700 (1997).
93. Mosser, J. et al. Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters. Nature 361, 726-730 (1993).
94. Wilson, P. J. et al. Hunter syndrome: isolation of an iduronate-2-sulfatase cDNA clone and analysis of patient DNA. Proc. Natl Acad. Sci. USA 21, 8531-8535 (1990).
95. Rosenthal, A., Jouet, M. & Kenwrick, S. Aberrant splicing of neural cell adhesion molecule L1 mRNA in a family with X-linked hydrocephalus. Nature Genet. 2, 107-112 (1992).
96. Jinnah, H. A. et al. The spectrum of inherited mutations causing HPRT deficiency: 75 new cases and a review of 196 previously reported cases. Mutat. Res. 3, 309-326 (2000).
97. Des Portes, V. et al. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92, 51-61 (1998).
98. Gleeson, J. G. et al. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92, 63-72 (1998).
99. Attree, O. et al. The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 358, 239-242 (1992).
100. Jin, H. et al. A novel X-linked gene, DDP, shows mutations in families with deafness (DFN-1), dystonia, mental deficiency and blindness. Nature Genet. 2, 177-180 (1996).
101. Quaderi, N. A. et al. Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nature Genet. 3, 285-291 (1997).
102. Vulpe, C. et al. Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nature Genet. 1, 7-13 (1993).
103. Chelly, J. et al. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nature Genet. 1, 14-19 (1993).
104. Batshaw, M. L., Roan, Y., Jung, A. L., Rosenberg, L. A. & Brusilow, S. W. Cerebral dysfunction in asymptomatic carriers of ornithine transcarbamylase deficiency. N. Engl. J. Med. 302, 482-485 (1980).
105. Lissens, W. et al. Mutations in the X-linked pyruvate dehydrogenase (E1) α subunit gene (PDHA1) in patients with a pyruvate dehydrogenase complex deficiency. Rev. Hum. Mutat. 15, 209-219 (2000).
106. Pasteris, N. G. et al. Isolation and characterization of the faciogenital dysplagia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell 79, 669-678 (1994).
107. Mitchell, J. R., Wood, E. & Collins, K. A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402, 551-555 (1999).
108. Pilia, G. et al. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nature Genet. 3, 241-247 (1996).
109. Felisari, G. et al. Loss of Dp140 dystrophin isoform and intellectual impairment in Duchenne dystrophy. Neurology 55, 559-564 (2000).
110. Smahi, A. et al. Genomic rearrangement in NEMO impairs NF-κB activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium. Nature 405, 466-472 (2000).
111. Meindl, A. et al. Norrie disease is caused by mutations in an extracellular protein resembling C-terminal globular domain of mucins. Nature Genet. 2, 139-143 (1992).
112. Cailloux, F. et al. Genotype-phenotype correlation in inherited brain myelination defects due to proteolipid protein gene mutations. Clinical European Network on Brain Dysmyelinating Disease. Eur. J. Hum. Genet. 11, 837-845 (2000).
113. Fox, J. W. et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia? Neuron 21, 1315-1325 (1998).