Cardiomyopathy is associated with ribosomal protein gene haplo-insufficiency in Drosophila melanogaster

Genetics

Volumn 189, Issue 3, 2011, Pages 861-870

  Casad, Michelle E ^a   Abraham, Dennis ^a   Kim, Il Man ^a   Frangakis, Stephan ^a   Dong, Brian ^a   Lin, Na ^a,b   Wolf, Matthew J ^a   Rockman, Howard A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CYTOPLASM; DROSOPHILA MELANOGASTER; GENE; GENE MUTATION; GENETIC DISORDER; HAPLOINSUFFICIENCY; HEART FUNCTION; HEART SIZE; MINUTE SYNDROME; MITOCHONDRION; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PRIORITY JOURNAL; RPS15AA GENE;

ANIMALS; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE DELETION; GENE KNOCKDOWN TECHNIQUES; HAPLOINSUFFICIENCY; RIBOSOMAL PROTEINS;

DROSOPHILA MELANOGASTER;

EID: 81255210733     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.131482     Document Type: Article

References (51)

1. Alexander, S., N. Woodling, and B. Yedvobnick, 2006 Insertional inactivation of the L13a ribosomal protein gene of Drosophila melanogaster identifies a new Minute locus. Gene 368: 46-52.
2. Allikian, M. J., G. Bhabha, P. Dospoy, A. Heydemann, P. Ryder et al., 2007 Reduced life span with heart and muscle dysfunction in Drosophila sarcoglycan mutants. Hum. Mol. Genet. 16: 2933-2943
3. Andersson, S., S. Saeboe-Larssen, A. Lambertsson, J. Merriam, and M. Jacobs-Lorena, 1994 A Drosophila third chromosome Minute locus encodes a ribosomal protein. Genetics 137: 513-520.
4. Bilanges, B., and D. Stokoe, 2007 Mechanisms of translational deregulation in human tumors and therapeutic intervention strategies. Oncogene 26: 5973-5990.
5. Da Costa, L., H. Moniz, M. Simansour, G. Tchernia, N. Mohandas et al., 2010 Diamond-Blackfan anemia, ribosome and erythropoiesis. Transfus. Clin. Biol. 17: 112-119.
6. Devlin, E. E., L. Dacosta, N. Mohandas, G. Elliott, and D. M. Bodine, 2010 A transgenic mouse model demonstrates a dominant negative effect of a point mutation in the RPS19 gene associated with Diamond-Blackfan anemia. Blood 116: 2826-2835.
7. Dietzl, G., D. Chen, F. Schnorrer, K. C. Su, Y. Barinova et al., 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156.
8. Doherty, L., M. R. Sheen, A. Vlachos, V. Choesmel, M. F. O'Donohue et al., 2010 Ribosomal protein genes RPS10 and RPS26 are commonly mutated in Diamond-Blackfan anemia. Am. J. Hum. Genet. 86: 222-228.
9. Draptchinskaia, N., P. Gustavsson, B. Andersson, M. Pettersson, T. N. Willig et al., 1999 The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat. Genet. 21: 169-175.
10. Duffy, J. B., J. Wells, and J. P. Gergen, 1996 Dosage-sensitive maternal modifiers of the Drosophila segmentation gene runt. Genetics 142: 839-852.
11. Fauvarque, M., P. Laurenti, A. Boivin, S. Bloyer, R. Griffin-Shea et al., 2001 Dominant modifiers of the polyhomeotic extrasex-combs phenotype induced by marked P element insertional mutagenesis in Drosophila. Genet. Res. 78: 137-148.
12. Freed, E. F., F. Bleichert, L. M. Dutca, and S. J. Baserga, 2010 When ribosomes go bad: diseases of ribosome biogenesis. Mol. Biosyst. 6: 481-493.
13. Frei, C., M. Galloni, E. Hafen, and B. A. Edgar, 2005 The Drosophila mitochondrial ribosomal protein mRpL12 is required for Cyclin D/Cdk4-driven growth. EMBO J. 24: 623-634.
14. Goldstein, J. A., S. M. Kelly, P. P. LoPresti, A. Heydemann, J. U. Earley et al., 2011 SMAD signaling drives heart and muscle dysfunction in a Drosophila model of muscular dystrophy. Hum. Mol. Genet. 20: 894-904.
15. Hart, K., T. Klein, and M. Wilcox, 1993 A Minute encoding a ribosomal protein enhances wing morphogenesis mutants. Mech. Dev. 43: 101-110.
16. Ito, E., Y. Konno, T. Toki, and K. Terui, 2010 Molecular pathogenesis in Diamond-Blackfan anemia. Int. J. Hematol. 92: 413-418.
17. Kim, I. M., and M. J. Wolf, 2009 Serial examination of an inducible and reversible dilated cardiomyopathy in individual adult Drosophila. PLoS One 4: e7132.
18. Kim, I. M., M. J. Wolf, and H. A. Rockman, 2010 Gene deletion screen for cardiomyopathy in adult Drosophila identifies a new notch ligand. Circ. Res. 106: 1233-1243.
19. Kondrashov, N., A. Pusic, C. R. Stumpf, K. Shimizu, A. C. Hsieh et al., 2011 Ribosome-mediated specificity in hox mRNA translation and vertebrate tissue patterning. Cell 145: 383-397.
20. Lambertsson, A., 1998 The minute genes in Drosophila and their molecular functions. Adv. Genet. 38: 69-134.
21. Marygold, S., C. Coelho, and S. Leevers, 2005 Genetic analysis of RpL38 and RpL5, two Minute genes located in the centric heterochromatin of chromosome 2 of Drosophila melanogaster. Genetics 169: 683-695.
22. Marygold, S. J., J. Roote, G. Reuter, A. Lambertsson, M. Ashburner et al., 2007 The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 8: R216.
23. McKim, K., J. Dahmus, and R. Hawley, 1996 Cloning of the Drosophila melanogaster meiotic recombination gene mei-218: a genetic and molecular analysis of interval 15E. Genetics 144: 215-228.
24. Miller, C., A. Saada, N. Shaul, N. Shabtai, E. Ben-Shalom et al., 2004 Defective mitochondrial translation caused by a ribosomal protein (MRPS16) mutation. Ann. Neurol. 56: 734-738.
25. Montanaro, L., D. Trere, and M. Derenzini, 2008 Nucleolus, ribosomes, and cancer. Am. J. Pathol. 173: 301-310.
26. Narla, A., and B. L. Ebert, 2010 Ribosomopathies: human disorders of ribosome dysfunction. Blood 115: 3196-3205.
27. Narla, A., S. N. Hurst, and B. L. Ebert, 2011 Ribosome defects in disorders of erythropoiesis. Int. J. Hematol. 93: 144-149.
28. Neely, G. G., K. Kuba, A. Cammarato, K. Isobe, S. Amann et al., 2010 A global in vivo Drosophila RNAi screen identifies NOT3 as a conserved regulator of heart function. Cell 141: 142-153.
29. Noben-Trauth, K., and J. R. Latoche, 2011 Ectopic mineralization in the middle ear and chronic otitis media with effusion caused by RPL38 deficiency in the Tail-short (Ts) mouse. J. Biol. Chem. 286: 3079-3093.
30. O'Brien, T. W., B. J. O'Brien, and R. A. Norman, 2005 Nuclear MRP genes and mitochondrial disease. Gene 354: 147-151.
31. Parks, A. L., K. R. Cook, M. Belvin, N. A. Dompe, R. Fawcett et al., 2004 Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36: 288-292.
32. Qian, L., and R. Bodmer, 2009 Partial loss of GATA factor Pannier impairs adult heart function in Drosophila. Hum. Mol. Genet. 18: 3153-3163.
33. Ruggero, D., and P. P. Pandolfi, 2003 Does the ribosome translate cancer? Nat. Rev. Cancer 3: 179-192.
34. Ryder, E., M. Ashburner, R. Bautista-Llacer, J. Drummond, J. Webster et al., 2007 The DrosDel Deletion Collection: a Drosophila genomewide chromosomal deficiency resource. Genetics 177: 615-629.
35. Saada, A., A. Shaag, S. Arnon, T. Dolfin, C. Miller et al., 2007 Antenatal mitochondrial disease caused by mitochondrial ribosomal protein (MRPS22) mutation. J. Med. Genet. 44: 784-786.
36. Saeboe-Larssen, S., and A. Lambertsson, 1996 A novel Drosophila Minute locus encodes ribosomal protein S13. Genetics 143: 877-885.
37. Saeboe-Larssen, S., B. Urbanczyk Mohebi, and A. Lambertsson, 1997 The Drosophila ribosomal protein L14-encoding gene, identified by a novel Minute mutation in a dense cluster of previously undescribed genes in cytogenetic region 66D. Mol. Gen. Genet. 255: 141-151.
38. Schmidt, A., M. Hollmann, and U. Schafer, 1996 A newly identified Minute locus, M(2)32D, encodes the ribosomal protein L9 in Drosophila melanogaster. Mol. Gen. Genet. 251: 381-387.
39. Smits, P., A. Saada, S. B. Wortmann, A. J. Heister, M. Brink et al., 2010 Mutation in mitochondrial ribosomal protein MRPS22 leads to Cornelia de Lange-like phenotype, brain abnormalities and hypertrophic cardiomyopathy. Eur. J. Hum. Genet. 19: 394-399.
40. Taghli-Lamallem, O., T. Akasaka, G. Hogg, U. Nudel, D. Yaffe et al., 2008 Dystrophin deficiency in Drosophila reduces lifespan and causes a dilated cardiomyopathy phenotype. Aging Cell 7: 237-249.
41. Thibault, S. T., M. A. Singer, W. Y. Miyazaki, B. Milash, N. A. Dompe et al., 2004 A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36: 283-287.
42. Torok, I., D. Herrmann-Horle, I. Kiss, G. Tick, G. Speer et al., 1999 Down-regulation of RpS21, a putative translation initiation factor interacting with P40, produces viable Minute imagos and larval lethality with overgrown hematopoietic organs and imaginal discs. Mol. Cell. Biol. 19: 2308-2321.
43. Tselykh, T. V., C. Roos, and T. I. Heino, 2005 The mitochondrial ribosome-specific MrpL55 protein is essential in Drosophila and dynamically required during development. Exp. Cell Res. 307: 354-366.
44. Tyler, D., W. Li, N. Zhuo, B. Pellock, and N. Baker, 2007 Genes affecting cell competition in Drosophila. Genetics 175: 643-657.
45. van Beest, M., M. Mortin, and H. Clevers, 1998 Drosophila RpS3a, a novel Minute gene situated between the segment polarity genes cubitus interruptus and dTCF. Nucleic Acids Res. 26: 4471-4475.
46. Warner, J. R., and K. B. McIntosh, 2009 How common are extraribosomal functions of ribosomal proteins? Mol. Cell 34: 3-11.
47. Wessells, R. J., E. Fitzgerald, J. R. Cypser, M. Tatar, and R. Bodmer, 2004 Insulin regulation of heart function in aging fruit flies. Nat. Genet. 36: 1275-1281.
48. Wolf, M. J., H. Amrein, J. A. Izatt, M. A. Choma, M. C. Reedy et al., 2006 Drosophila as a model for the identification of genes causing adult human heart disease. Proc. Natl. Acad. Sci. USA 103: 1394-1399.
49. Yin, Z., and M. Frasch, 1998 Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. Dev. Genet. 22: 187-200.
50. Yu, L., T. Lee, N. Lin, and M. J. Wolf, 2010 Affecting Rhomboid-3 function causes a dilated heart in adult Drosophila. PLoS Genet. 6: e1000969.
51. Zhan, Y., N. Y. Melian, M. Pantoja, N. Haines, H. Ruohola-Baker et al., 2010 Dystroglycan and mitochondrial ribosomal protein l34 regulate differentiation in the Drosophila eye. PLoS One 5: e10488.