tRNA Methyltransferase Homolog Gene TRMT10A Mutation in Young Onset Diabetes and Primary Microcephaly in Humans

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Igoillo Esteve, Mariana ^a   Genin, Anne ^a   Lambert, Nelle ^a,b   Désir, Julie ^a   Pirson, Isabelle ^a   Abdulkarim, Baroj ^a   Simonis, Nicolas ^a   Drielsma, Anais ^a   Marselli, Lorella ^c   Marchetti, Piero ^c   Vanderhaeghen, Pierre ^a   Eizirik, Décio L ^a   Wuyts, Wim ^d   Julier, Cécile ^e,f   Chakera, Ali J ^g   Ellard, Sian ^g   Hattersley, Andrew T ^g   Abramowicz, Marc ^a,b   Cnop, Miriam ^a,b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b ERASME HOSPITAL   (Belgium)

^c Central Laboratory   (Italy)

^d ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^e INSERM   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA METHYLTRANSFERASE; METHYLTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN; TRM10 PROTEIN, S CEREVISIAE; TRMT10A PROTEIN, HUMAN;

ADULT; APOPTOSIS; ARTICLE; CASE REPORT; CELLULAR DISTRIBUTION; CLINICAL FEATURE; CONSANGUINITY; EXON; FAMILY STUDY; FEMALE; GENE; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; GENE SILENCING; GENOTYPE; HAPLOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; LINKAGE ANALYSIS; MICROCEPHALY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONSENSE MUTATION; NUCLEOLUS; PANCREAS ISLET BETA CELL; PATHOGENESIS; SIBLING; SINGLE NUCLEOTIDE POLYMORPHISM; TRMT10A GENE; ANIMAL; COMPLICATION; DEFICIENCY; GENETIC LINKAGE; GENETICS; INTELLECTUAL IMPAIRMENT; MALE; METABOLISM; MUTATION; ONSET AGE; PATHOLOGY; PEDIGREE; RAT;

ADULT; AGE OF ONSET; ANIMALS; APOPTOSIS; DIABETES MELLITUS, TYPE 2; FEMALE; GENETIC LINKAGE; HUMANS; INSULIN-SECRETING CELLS; INTELLECTUAL DISABILITY; MALE; METHYLTRANSFERASES; MICROCEPHALY; MUTATION; PEDIGREE; RATS; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES;

EID: 84887300561     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003888     Document Type: Article

References (70)

1. Zimmet P, Alberti KG, Shaw J, (2001) Global and societal implications of the diabetes epidemic. Nature 414: 782-787.
2. Stumvoll M, Goldstein BJ, van Haeften TW, (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365: 1333-1346.
3. Cnop M, (2008) Fatty acids and glucolipotoxicity in the pathogenesis of Type 2 diabetes. Biochem Soc Trans 36: 348-352.
4. Ferrannini E, (1998) Insulin resistance versus insulin deficiency in non-insulin-dependent diabetes mellitus: problems and prospects. Endocr Rev 19: 477-490.
5. Gerich JE, (1998) The genetic basis of type 2 diabetes mellitus: impaired insulin secretion versus impaired insulin sensitivity. Endocr Rev 19: 491-503.
6. Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, et al. (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316: 1331-1336.
7. Morris AP, Voight BF, Teslovich TM, Ferreira T, Segre AV, et al. (2012) Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat Genet 44: 981-990.
8. Dehwah MA, Wang M, Huang QY, (2010) CDKAL1 and type 2 diabetes: a global meta-analysis. Genet Mol Res 9: 1109-1120.
9. Wei FY, Suzuki T, Watanabe S, Kimura S, Kaitsuka T, et al. (2011) Deficit of tRNA(Lys) modification by Cdkal1 causes the development of type 2 diabetes in mice. J Clin Invest 121: 3598-3608.
10. Sprinzl M, Vassilenko KS, (2005) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 33: D139-140.
11. Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S, (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 26: 148-153.
12. Towns WL, Begley TJ, (2012) Transfer RNA methytransferases and their corresponding modifications in budding yeast and humans: activities, predications, and potential roles in human health. DNA Cell Biol 31: 434-454.
13. Urbonavicius J, Qian Q, Durand JM, Hagervall TG, Bjork GR, (2001) Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J 20: 4863-4873.
14. Phizicky EM, Hopper AK, (2010) tRNA biology charges to the front. Genes Dev 24: 1832-1860.
15. Agris PF, (2004) Decoding the genome: a modified view. Nucleic Acids Res 32: 223-238.
16. Jackman JE, Montange RK, Malik HS, Phizicky EM, (2003) Identification of the yeast gene encoding the tRNA m1G methyltransferase responsible for modification at position 9. RNA 9: 574-585.
17. Gustavsson M, Ronne H, (2008) Evidence that tRNA modifying enzymes are important in vivo targets for 5-fluorouracil in yeast. RNA 14: 666-674.
18. Buhler M, Mohn F, Stalder L, Muhlemann O, (2005) Transcriptional silencing of nonsense codon-containing immunoglobulin minigenes. Mol Cell 18: 307-317.
19. Chang YF, Imam JS, Wilkinson MF, (2007) The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76: 51-74.
20. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585-587.
21. Kosugi S, Hasebe M, Tomita M, Yanagawa H, (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A 106: 10171-10176.
22. Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E, et al. (2009) Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 284: 478-485.
23. Ochs RL, Lischwe MA, Spohn WH, Busch H, (1985) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54: 123-133.
24. Cnop M, Foufelle F, Velloso LA, (2012) Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med 18: 59-68.
25. Cunha DA, Hekerman P, Ladriere L, Bazarra-Castro A, Ortis F, et al. (2008) Initiation and execution of lipotoxic ER stress in pancreatic β-cells. J Cell Sci 121: 2308-2318.
26. Berg M, Agesen TH, Thiis-Evensen E, Merok MA, Teixeira MR, et al. (2010) Distinct high resolution genome profiles of early onset and late onset colorectal cancer integrated with gene expression data identify candidate susceptibility loci. Mol Cancer 9: 100.
27. Thompson M, Haeusler RA, Good PD, Engelke DR, (2003) Nucleolar clustering of dispersed tRNA genes. Science 302: 1399-1401.
28. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
29. Melton DA, De Robertis EM, Cortese R, (1980) Order and intracellular location of the events involved in the maturation of a spliced tRNA. Nature 284: 143-148.
30. Simos G, Tekotte H, Grosjean H, Segref A, Sharma K, et al. (1996) Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J 15: 2270-2284.
31. Rose AM, Joyce PB, Hopper AK, Martin NC, (1992) Separate information required for nuclear and subnuclear localization: additional complexity in localizing an enzyme shared by mitochondria and nuclei. Mol Cell Biol 12: 5652-5658.
32. Mei Y, Yong J, Stonestrom A, Yang X, (2010) tRNA and cytochrome c in cell death and beyond. Cell Cycle 9: 2936-2939.
33. Hou YM, Yang X, (2013) Regulation of cell death by tRNA. Antioxid Redox Signal 19: 583-94.
34. Passemard S, Titomanlio L, Elmaleh M, Afenjar A, Alessandri JL, et al. (2009) Expanding the clinical and neuroradiologic phenotype of primary microcephaly due to ASPM mutations. Neurology 73: 962-969.
35. Woods CG, (2004) Human microcephaly. Curr Opin Neurobiol 14: 112-117.
36. Genin A, Desir J, Lambert N, Biervliet M, Van Der Aa N, et al. (2012) Kinetochore KMN network gene CASC5 mutated in primary microcephaly. Hum Mol Genet 21: 5306-5317.
37. de Wit MC, de Coo IF, Julier C, Delepine M, Lequin MH, et al. (2006) Microcephaly and simplified gyral pattern of the brain associated with early onset insulin-dependent diabetes mellitus. Neurogenetics 7: 259-263.
38. Poulton CJ, Schot R, Kia SK, Jones M, Verheijen FW, et al. (2011) Microcephaly with simplified gyration, epilepsy, and infantile diabetes linked to inappropriate apoptosis of neural progenitors. Am J Hum Genet 89: 265-276.
39. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, et al. (2000) EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 25: 406-409.
40. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D, (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5: 897-904.
41. Namavar Y, Barth PG, Poll-The BT, Baas F, (2011) Classification, diagnosis and potential mechanisms in pontocerebellar hypoplasia. Orphanet J Rare Dis 6: 50.
42. Khan MA, Rafiq MA, Noor A, Hussain S, Flores JV, et al. (2012) Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. Am J Hum Genet 90: 856-863.
43. Abbasi-Moheb L, Mertel S, Gonsior M, Nouri-Vahid L, Kahrizi K, et al. (2012) Mutations in NSUN2 cause autosomal-recessive intellectual disability. Am J Hum Genet 90: 847-855.
44. Najmabadi H, Hu H, Garshasbi M, Zemojtel T, Abedini SS, et al. (2011) Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature 478: 57-63.
45. Arragain S, Handelman SK, Forouhar F, Wei FY, Tomizawa K, et al. (2010) Identification of eukaryotic and prokaryotic methylthiotransferase for biosynthesis of 2-methylthio-N6-threonylcarbamoyladenosine in tRNA. J Biol Chem 285: 28425-28433.
46. Sambrook J, Russel DW (2001) Preparation and analysis of eukaryotic genomic DNA. Molecular cloning-a laboratory manual. 3rd edition. New York: Cold Spring Harbor Laboratory Press. pp. 6.4-6.12.
47. Woods CG, Valente EM, Bond J, Roberts E, (2004) A new method for autozygosity mapping using single nucleotide polymorphisms (SNPs) and EXCLUDEAR. J Med Genet 41: e101.
48. Kruglyak L, Daly MJ, Lander ES, (1995) Rapid multipoint linkage analysis of recessive traits in nuclear families, including homozygosity mapping. Am J Hum Genet 56: 519-527.
49. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
50. Li R, Li Y, Fang X, Yang H, Wang J, et al. (2009) SNP detection for massively parallel whole-genome resequencing. Genome Res 19: 1124-1132.
51. Lee JW, Kim WH, Lim JH, Song EH, Song J, et al. (2009) Mitochondrial dysfunction: glucokinase downregulation lowers interaction of glucokinase with mitochondria, resulting in apoptosis of pancreatic beta-cells. Cell Signal 21: 69-78.
52. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
53. Lambert N, Lambot MA, Bilheu A, Albert V, Englert Y, et al. (2011) Genes expressed in specific areas of the human fetal cerebral cortex display distinct patterns of evolution. PLoS One 6: e17753.
54. Asfari M, Janjic D, Meda P, Li G, Halban PA, et al. (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130: 167-178.
55. Ortis F, Cardozo AK, Crispim D, Storling J, Mandrup-Poulsen T, et al. (2006) Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-κB activation. Mol Endocrinol 20: 1867-1879.
56. Rasschaert J, Ladriere L, Urbain M, Dogusan Z, Katabua B, et al. (2005) Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA+ interferon-γ-induced apoptosis in primary pancreatic β-cells. J Biol Chem 280: 33984-33991.
57. Ling Z, Hannaert JC, Pipeleers D, (1994) Effect of nutrients, hormones and serum on survival of rat islet β-cells in culture. Diabetologia 37: 15-21.
58. Lupi R, Dotta F, Marselli L, Del Guerra S, Masini M, et al. (2002) Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 51: 1437-1442.
59. Moore F, Colli ML, Cnop M, Esteve MI, Cardozo AK, et al. (2009) PTPN2, a candidate gene for type 1 diabetes, modulates interferon-γ-induced pancreatic β-cell apoptosis. Diabetes 58: 1283-1291.
60. Igoillo-Esteve M, Marselli L, Cunha DA, Ladriere L, Ortis F, et al. (2010) Palmitate induces a pro-inflammatory response in human pancreatic islets that mimics CCL2 expression by beta cells in type 2 diabetes. Diabetologia 53: 1395-1405.
61. Cnop M, Igoillo-Esteve M, Rai M, Begu A, Serroukh Y, et al. (2012) Central role and mechanisms of β-cell dysfunction and death in Friedreich ataxia-associated diabetes. Ann Neurol 72: 971-982.
62. Ladriere L, Igoillo-Esteve M, Cunha DA, Brion JP, Bugliani M, et al. (2010) Enhanced signaling downstream of ribonucleic acid-activated protein kinase-like endoplasmic reticulum kinase potentiates lipotoxic endoplasmic reticulum stress in human islets. J Clin Endocrinol Metab 95: 1442-1449.
63. Cunha DA, Igoillo-Esteve M, Gurzov EN, Germano CM, Naamane N, et al. (2012) Death protein 5 and p53-upregulated modulator of apoptosis mediate the endoplasmic reticulum stress-mitochondrial dialog triggering lipotoxic rodent and human β-cell apoptosis. Diabetes 61: 2763-2775.
64. Kharroubi I, Ladriere L, Cardozo AK, Dogusan Z, Cnop M, et al. (2004) Free fatty acids and cytokines induce pancreatic β-cell apoptosis by different mechanisms: role of nuclear factor-κB and endoplasmic reticulum stress. Endocrinology 145: 5087-5096.
65. Overbergh L, Valckx D, Waer M, Mathieu C, (1999) Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 11: 305-312.
66. Olerud J, Johansson M, Lawler J, Welsh N, Carlsson PO, (2008) Improved vascular engraftment and graft function after inhibition of the angiostatic factor thrombospondin-1 in mouse pancreatic islets. Diabetes 57: 1870-1877.
67. Olsson R, Carlsson PO, (2005) Better vascular engraftment and function in pancreatic islets transplanted without prior culture. Diabetologia 48: 469-476.
68. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG, (2001) Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 50: 1771-1777.
69. Cross BC, Bond PJ, Sadowski PG, Jha BK, Zak J, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A 109: E869-878.
70. Cnop M, Ladriere L, Hekerman P, Ortis F, Cardozo AK, et al. (2007) Selective inhibition of eukaryotic translation initiation factor 2α dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic β-cell dysfunction and apoptosis. J Biol Chem 282: 3989-3997.