A Syndromic Intellectual Disability Disorder Caused by Variants in TELO2, a Gene Encoding a Component of the TTT Complex

American Journal of Human Genetics

Volumn 98, Issue 5, 2016, Pages 909-918

  You, Jing ^a   Sobreira, Nara L ^a   Gable, Dustin L ^a   Jurgens, Julie ^a   Grange, Dorothy K ^b   Belnap, Newell ^c   Siniard, Ashley ^c   Szelinger, Szabolcs ^c   Schrauwen, Isabelle ^c   Richholt, Ryan F ^c   Vallee, Stephanie E ^d   Dinulos, Mary Beth P ^d,e   Valle, David ^a   Armanios, Mary ^a   Hoover Fong, Julie ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^d DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; CARRIER PROTEIN; CHAPERONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; TELOMERE BINDING PROTEIN; TTI1 PROTEIN, HUMAN; TTI2 PROTEIN, HUMAN;

ADOLESCENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHILD; CLEFT PALATE; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE FREQUENCY; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENETIC STABILITY; GENETIC VARIATION; HEARING IMPAIRMENT; HETEROZYGOSITY; HETEROZYGOTE; HOMOZYGOSITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTELLECTUAL IMPAIRMENT; MALE; MICROCEPHALY; MISSENSE MUTATION; NONSENSE MEDIATED MRNA DECAY; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PERIPHERAL LYMPHOCYTE; PRESCHOOL CHILD; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD; STEADY STATE; SURVIVAL; TELO2 GENE; TELOMERE; VISUAL IMPAIRMENT; GENETICS; INTELLECTUAL DISABILITY; PEDIGREE;

ADOLESCENT; CARRIER PROTEINS; CHILD; FEMALE; HUMANS; INTELLECTUAL DISABILITY; MALE; MOLECULAR CHAPERONES; PEDIGREE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-SERINE-THREONINE KINASES; TELOMERE-BINDING PROTEINS;

EID: 84964664169     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.03.014     Document Type: Article

References (55)

1. R.L. Schalock, R.A. Luckasson, K.A. Shogren, S. Borthwick-Duffy, V. Bradley, W.H. Buntinx, D.L. Coulter, E.M. Craig, S.C. Gomez, Y. Lachapelle, and et al. The renaming of mental retardation: understanding the change to the term intellectual disability Intellect. Dev. Disabil. 45 2007 116 124
2. H.H. Ropers Genetics of early onset cognitive impairment Annu. Rev. Genomics Hum. Genet. 11 2010 161 187
3. L. Musante, and H.H. Ropers Genetics of recessive cognitive disorders Trends Genet. 30 2014 32 39
4. A.J. Lustig, and T.D. Petes Identification of yeast mutants with altered telomere structure Proc. Natl. Acad. Sci. USA 83 1986 1398 1402
5. K.W. Runge, and V.A. Zakian TEL2, an essential gene required for telomere length regulation and telomere position effect in Saccharomyces cerevisiae Mol. Cell. Biol. 16 1996 3094 3105
6. K.E. Hurov, C. Cotta-Ramusino, and S.J. Elledge A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability Genes Dev. 24 2010 1939 1950
7. H. Takai, R.C. Wang, K.K. Takai, H. Yang, and T. de Lange Tel2 regulates the stability of PI3K-related protein kinases Cell 131 2007 1248 1259
8. Y. Kakihara, and W.A. Houry The R2TP complex: discovery and functions Biochim. Biophys. Acta 1823 2012 101 107
9. M. Pal, M. Morgan, S.E. Phelps, S.M. Roe, S. Parry-Morris, J.A. Downs, S. Polier, L.H. Pearl, and C. Prodromou Structural basis for phosphorylation-dependent recruitment of Tel2 to Hsp90 by Pih1 Structure 22 2014 805 818
10. R.T. Abraham Cell cycle checkpoint signaling through the ATM and ATR kinases Genes Dev. 15 2001 2177 2196
11. M.B. Kastan, and J. Bartek Cell-cycle checkpoints and cancer Nature 432 2004 316 323
12. L. Woodbine, J.A. Neal, N.-K. Sasi, M. Shimada, K. Deem, H. Coleman, W.B. Dobyns, T. Ogi, K. Meek, E.G. Davies, and P.A. Jeggo PRKDC mutations in a SCID patient with profound neurological abnormalities J. Clin. Invest. 123 2013 2969 2980
13. S. Wullschleger, R. Loewith, and M.N. Hall TOR signaling in growth and metabolism Cell 124 2006 471 484
14. E. Conti, and E. Izaurralde Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species Curr. Opin. Cell Biol. 17 2005 316 325
15. A. Yamashita, T. Ohnishi, I. Kashima, Y. Taya, and S. Ohno Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay Genes Dev. 15 2001 2215 2228
16. Z. Herceg, and Z.Q. Wang Rendez-vous at mitosis: TRRAPed in the chromatin Cell Cycle 4 2005 383 387
17. S.B. McMahon, H.A. Van Buskirk, K.A. Dugan, T.D. Copeland, and M.D. Cole The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins Cell 94 1998 363 374
18. N. Sandoval, M. Platzer, A. Rosenthal, T. Dörk, R. Bendix, B. Skawran, M. Stuhrmann, R.D. Wegner, K. Sperling, S. Banin, and et al. Characterization of ATM gene mutations in 66 ataxia telangiectasia families Hum. Mol. Genet. 8 1999 69 79
19. A. Shanske, D.G. Caride, L. Menasse-Palmer, A. Bogdanow, and R.W. Marion Central nervous system anomalies in Seckel syndrome: report of a new family and review of the literature Am. J. Med. Genet. 70 1997 155 158
20. M. van der Burg, H. Ijspeert, N.S. Verkaik, T. Turul, W.W. Wiegant, K. Morotomi-Yano, P.O. Mari, I. Tezcan, D.J. Chen, M.Z. Zdzienicka, and et al. A DNA-PKcs mutation in a radiosensitive T-B- SCID patient inhibits Artemis activation and nonhomologous end-joining J. Clin. Invest. 119 2009 91 98
21. G. Baynam, A. Overkov, M. Davis, K. Mina, L. Schofield, R. Allcock, N. Laing, M. Cook, H. Dawkins, and J. Goldblatt A germline MTOR mutation in Aboriginal Australian siblings with intellectual disability, dysmorphism, macrocephaly, and small thoraces Am. J. Med. Genet. A. 167 2015 1659 1667
22. L.D. Smith, C.J. Saunders, D.L. Dinwiddie, A.M. Altherton, N.A. Miller, S.E. Soden, E.G. Farrow, A.T. Abdelmoity, and S.F. Kingsmore Exome sequencing reveals de novo germline mutation of the mammalian target of rapamycin (MTOR) in a patient with megalencephaly and intractable seizures J Genomes Exomes 2 2013 63 72
23. D.A. Guertin, and D.M. Sabatini Defining the role of mTOR in cancer Cancer Cell 12 2007 9 22
24. X. Wei, V. Walia, J.C. Lin, J.K. Teer, T.D. Prickett, J. Gartner, S. Davis, K. Stemke-Hale, M.A. Davies, J.E. Gershenwald, et al. NISC Comparative Sequencing Program Exome sequencing identifies GRIN2A as frequently mutated in melanoma Nat. Genet. 43 2011 442 446
25. M.A. Nikiforov, S. Chandriani, J. Park, I. Kotenko, D. Matheos, A. Johnsson, S.B. McMahon, and M.D. Cole TRRAP-dependent and TRRAP-independent transcriptional activation by Myc family oncoproteins Mol. Cell. Biol. 22 2002 5054 5063
26. Z. Herceg, W. Hulla, D. Gell, C. Cuenin, M. Lleonart, S. Jackson, and Z.Q. Wang Disruption of Trrap causes early embryonic lethality and defects in cell cycle progression Nat. Genet. 29 2001 206 211
27. N. Sobreira, F. Schiettecatte, C. Boehm, D. Valle, and A. Hamosh New tools for Mendelian disease gene identification: PhenoDB variant analysis module; and GeneMatcher, a web-based tool for linking investigators with an interest in the same gene Hum. Mutat. 36 2015 425 431
28. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
29. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, and M.A. DePristo The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res. 20 2010 1297 1303
30. M.A. DePristo, E. Banks, R. Poplin, K.V. Garimella, J.R. Maguire, C. Hartl, A.A. Philippakis, G. del Angel, M.A. Rivas, M. Hanna, and et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data Nat. Genet. 43 2011 491 498
31. D.M. Altshuler, R.A. Gibbs, L. Peltonen, D.M. Altshuler, R.A. Gibbs, L. Peltonen, E. Dermitzakis, S.F. Schaffner, F. Yu, L. Peltonen, et al. International HapMap 3 Consortium Integrating common and rare genetic variation in diverse human populations Nature 467 2010 52 58
32. L. Zhang, C. Jie, C. Obie, F. Abidi, C.E. Schwartz, R.E. Stevenson, D. Valle, and T. Wang X chromosome cDNA microarray screening identifies a functional PLP2 promoter polymorphism enriched in patients with X-linked mental retardation Genome Res. 17 2007 641 648
33. T.J. Hubbard, B.L. Aken, S. Ayling, B. Ballester, K. Beal, E. Bragin, S. Brent, Y. Chen, P. Clapham, L. Clarke, and et al. Ensembl 2009 Nucleic Acids Res. 37 2009 D690 D697
34. G.R. Abecasis, A. Auton, L.D. Brooks, M.A. DePristo, R.M. Durbin, R.E. Handsaker, H.M. Kang, G.T. Marth, G.A. McVean 1000 Genomes Project Consortium An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
35. G.R. Abecasis, D. Altshuler, A. Auton, L.D. Brooks, R.M. Durbin, R.A. Gibbs, M.E. Hurles, G.A. McVean, G.A.T. McVean 1000 Genomes Project Consortium A map of human genome variation from population-scale sequencing Nature 467 2010 1061 1073
36. G.M. Baerlocher, I. Vulto, G. de Jong, and P.M. Lansdorp Flow cytometry and FISH to measure the average length of telomeres (flow FISH) Nat. Protoc. 1 2006 2365 2376
37. A.D. Auerbach Diagnosis of Fanconi anemia by diepoxybutane analysis Curr. Protoc. Hum. Genet. 85 2015 1 17
38. M.B. Penno, M. Pedrotti-Krueger, and T. Ray Cryopreservation of whole blood and isolated lymphocytes for B-cell imortalization J. Tiss. Cult. Meth. 15 1993 43 48
39. X. Sun, S.G. Becker-Catania, H.H. Chun, M.J. Hwang, Y. Huo, Z. Wang, M. Mitui, O. Sanal, L. Chessa, B. Crandall, and R.A. Gatti Early diagnosis of ataxia-telangiectasia using radiosensitivity testing J. Pediatr. 140 2002 724 731
40. F.O. Pinto, T. Leblanc, D. Chamousset, G. Le Roux, B. Brethon, B. Cassinat, J. Larghero, J.P. de Villartay, D. Stoppa-Lyonnet, A. Baruchel, and et al. Diagnosis of Fanconi anemia in patients with bone marrow failure Haematologica 94 2009 487 495
41. N. Izumi, A. Yamashita, H. Hirano, and S. Ohno Heat shock protein 90 regulates phosphatidylinositol 3-kinase-related protein kinase family proteins together with the RUVBL1/2 and Tel2-containing co-factor complex Cancer Sci. 103 2012 50 57
42. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, and et al. Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
43. S.T. Sherry, M.-H. Ward, M. Kholodov, J. Baker, L. Phan, E.M. Smigielski, and K. Sirotkin dbSNP: the NCBI database of genetic variation Nucleic Acids Res. 29 2001 308 311
44. I.A. Adzhubei, S. Schmidt, L. Peshkin, V.E. Ramensky, A. Gerasimova, P. Bork, A.S. Kondrashov, and S.R. Sunyaev A method and server for predicting damaging missense mutations Nat. Methods 7 2010 248 249
45. N.-L. Sim, P. Kumar, J. Hu, S. Henikoff, G. Schneider, and P.C. Ng SIFT web server: predicting effects of amino acid substitutions on proteins Nucleic Acids Res. 40 2012 W452 W457
46. P. Kumar, S. Henikoff, and P.C. Ng Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm Nat. Protoc. 4 2009 1073 1081
47. Z. Horejsí, H. Takai, C.A. Adelman, S.J. Collis, H. Flynn, S. Maslen, J.M. Skehel, T. de Lange, and S.J. Boulton CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability Mol. Cell 39 2010 839 850
48. T. Kaizuka, T. Hara, N. Oshiro, U. Kikkawa, K. Yonezawa, K. Takehana, S. Iemura, T. Natsume, and N. Mizushima Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly J. Biol. Chem. 285 2010 20109 20116
49. H. Takai, Y. Xie, T. de Lange, and N.P. Pavletich Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes Genes Dev. 24 2010 2019 2030
50. P.S. Hartman, and R.K. Herman Radiation-sensitive mutants of Caenorhabditis elegans Genetics 102 1982 159 178
51. B. Lakowski, and S. Hekimi Determination of life-span in Caenorhabditis elegans by four clock genes Science 272 1996 1010 1013
52. M. Shikata, F. Ishikawa, and J. Kanoh Tel2 is required for activation of the Mrc1-mediated replication checkpoint J. Biol. Chem. 282 2007 5346 5355
53. H. Najmabadi, H. Hu, M. Garshasbi, T. Zemojtel, S.S. Abedini, W. Chen, M. Hosseini, F. Behjati, S. Haas, P. Jamali, and et al. Deep sequencing reveals 50 novel genes for recessive cognitive disorders Nature 478 2011 57 63
54. M. Langouët, A. Saadi, G. Rieunier, S. Moutton, K. Siquier-Pernet, M. Fernet, P. Nitschke, A. Munnich, M.H. Stern, M. Chaouch, and L. Colleaux Mutation in TTI2 reveals a role for triple T complex in human brain development Hum. Mutat. 34 2013 1472 1476
55. J.A. Troca-Marín, J.J. Casañas, I. Benito, and M.L. Montesinos The Akt-mTOR pathway in Down's syndrome: the potential use of rapamycin/rapalogs for treating cognitive deficits CNS Neurol. Disord. Drug Targets 13 2014 34 40