Substitution of critical isoleucines in the KH domains of Drosophila fragile X protein results in partial loss-of-function phenotypes

Genetics

Volumn 175, Issue 3, 2007, Pages 1241-1250

  Banerjee, Paromita ^a   Nayar, Shweta ^a   Hebbar, Sarita ^a,c   Fox, Catherine F ^a,d   Jacobs, Michele C ^a,e   Park, Jae H ^b   Fernandes, Joyce J ^a   Dockendorff, Thomas C ^a  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; FRAGILE X MENTAL RETARDATION PROTEIN; ISOLEUCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; FEMALE; FUNCTIONAL ASSESSMENT; MALE; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANALYSIS OF VARIANCE; ANIMALS; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FRAGILE X MENTAL RETARDATION PROTEIN; IMMUNOHISTOCHEMISTRY; ISOLEUCINE; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; POINT MUTATION; RIBONUCLEOPROTEINS; RNA; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 34249079982     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.068908     Document Type: Article

References (59)

1. ADINOLFI, S., C. BAGNI, G. MUSCO, T. GIBSON, L. MAZZARELLA et al., 1999 Dissecting FMR1, the protein responsible for fragile X syndrome, in its structural and functional domains. RNA 5: 1248-1258.
2. ADINOLFI, S., A. RAMOS, S. R. MARTIN, F. DAL PIAZ, P. PUCCI et al., 2003 The N-terminus of the fragile X mental retardation protein contains a novel domain involved in dimerization and RNA binding. Biochemistry 42: 10437-10444.
3. ASHLEY, C. T., JR., K. D. WILKINSON, D. REINES and S. T. WARREN, 1993 FMR1 protein: conserved RNP family domains and selective RNA binding. Science 262: 563-566.
4. BAGNI, C., and W. T. GREENOUGH, 2005 From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat. Rev. Neurosci. 6: 376-387.
5. BARDONI, B., and J. L. MANDEL, 2002 Advances in understanding of fragile X pathogenesis and FMRP function, and in identification of X linked mental retardation genes. Curr. Opin. Genet. Dev. 12: 284-293.
6. BROWN, V., P. JIN, S. CEMAN, J. C. DARNELL, W. T. O'DONNELL et al., 2001 Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107: 477-487.
7. CAUDY, A. A., M. MYERS, G. J. HANNON and S. M. HAMMOND, 2002 Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16: 2491-2496.
8. CEMAN, S., V. BROWN and S. T. WARREN, 1999 Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Mol. Cell. Biol. 19: 7925-7932.
9. COSTA, A., Y. WANG, T. C. DOCKENDORFF, H. ERDJUMENT-BROMAGE, P. TEMPST et al., 2005 The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. Dev. Cell 8: 331-342.
10. DARNELL, J. C., K. B. JENSEN, P. JIN, V. BROWN, S. T. WARREN et al., 2001 Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107: 489-499.
11. DARNELL, J. C., C. E. FRASER, O. MOSTOVETSKY, G. STEFANI, T. A. JONES et al., 2005 Kissing complex RNAs mediate interaction between the fragile-X mental retardation protein KH2 domain and brain polyribosomes. Genes Dev. 19: 903-918.
12. DE BOULLE, K., A. J. VERKERK, E. REYNIERS, L. VITS, J. HENDRICKX et al., 1993 A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nat. Genet. 3: 31-35.
13. DESHPANDE, G., G. CALHOUN and P. SCHEDL, 2006 The Drosophila fragile X protein dFMR1 is required during early embryogenesis for pole cell formation and rapid nuclear division cycles. Genetics 174: 1287-1298.
14. DOCKENDORFF, T. C., H. S. SU, S. M. J. MCBRIDE, Z. YANG, C. H. CHOI et al., 2002 Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34: 973-984.
15. DÖLEN, G., and M. F. BEAR, 2005 Courting a cure for fragile X. Neuron 45: 642-644.
16. FENG, Y., D. ABSHER, D. E. EBERHART, V. BROWN, H. E. MALTER et al., 1997 FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1: 109-118.
17. GAO, F.-B., 2002 Understanding fragile X syndrome: insights from retarded flies. Neuron 34: 859-862.
18. GREENSPAN, R. J., and J. F. FERVEUR, 2000 Courtship in Drosophila. Annu. Rev. Genet. 34: 205-232.
19. HALL, J. C., 1994 The mating of a fly. Science 264: 1702-1714.
20. INOUE, S., M. SHIMODA, I. NISHINOKUBI, M. C. SIOMI, M. OKAMURA et al., 2002 A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 12: 1331-1335.
21. ISHIZUKA, A., M. C. SIOMI and H. SIOMI, 2002 A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16: 2497-2508.
22. JIN, P., and S. T. WARREN, 2003 New insights into fragile X syndrome: from molecules to neurobehaviors. Trends Biochem. Sci. 28: 152-158.
23. JIN, P., R. S. ALISCH and S. T. WARREN, 2004a RNA and microRNAs in fragile X mental retardation. Nat. Cell Biol. 6: 1048-1053.
24. JIN, P., D. C. ZARNESCU, S. CEMAN, M. NAKAMOTO, J. MOWREY et al., 2004b Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat. Neurosci. 7: 113-117.
25. LAGGERBAUER, B., D. OSTARECK, E. M. KEIDEL, A. OSTARECK-LEDERER and U. FISCHER, 2001 Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10: 329-338.
26. LEE, A., W. LI, K. XU, B. A. BOGERT, K. SU et al., 2003 Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130: 5543-5552.
27. LEWIS, H. A., K. MUSUNURU, K. B. JENSEN, C. EDO, H. CHEN et al., 2000 Sequence-specific RNA binding by a Nova KH domain: implications for paraneoplastic disease and the fragile X syndrome. Cell 100: 323-332.
28. LIPPMAN, Z., and R. MARTIENSSEN, 2004 The role of RNA interference in heterochromatic silencing. Nature 431: 364-370.
29. MATZKE, M. A., and J. A. BIRCHLER, 2005 RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6: 24-35.
30. MAURER-STROH, S., N. J. DICKENS, L. HUGHES-DAVIES, T. KOUZARIDES, F. EISENHABER et al., 2003 The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 28: 69-74.
31. MAZROUI, R., M. E. HUOT, S. TREMBLAY, N. BOILARD, Y. LABELLE, et al., 2003 Fragile X mental retardation protein determinants required for its association with polyribosomal mRNPs. Hum. Mol. Genet. 12: 3087-3096.
32. MCBRIDE, S. M. J., C. H. CHOI, Y. WANG, D. LIEBELT, E. BRAUNSTEIN et al., 2005 Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45: 753-764.
33. MICHEL, C. I., R. KRAFT and L. L. RESTIFO, 2004 Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24: 5798-5809.
34. MIYASHIRO, K. Y., A. BECKEL-MITCHENER, T. P. PURK, K. G. BECKER, T. BARRET et al., 2003 RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37: 417-431.
35. MORALES, J., P. R. HIESINGER, A. J. SCHROEDER, K. KUME, P. VERSTREKEN et al., 2002 Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34: 961-972.
36. MUSCO, G., G. STIER, C. JOSEPH, M. A. C. MORELLI, M. NILGES et al., 1996 Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell 85: 237-245.
37. MUSCO, G., A. KHARRAT, G. STIER, F. FRATERNALI, T. J. GIBSON et al., 1997 The solution structure of the first KH domain of FMR1, the protein responsible for the fragile X syndrome. Nat. Struct. Biol. 4: 712-716.
38. O'DONNELL, W. T., and S. T. WARREN, 2002 A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 25: 315-338.
39. PAL-BHADRA, M., B. A. LEIBOVITCH, S. G. GANDHI, M. RAO, U. BHADRA et al., 2004 Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669-672.
40. PAN, L., Y. Q. ZHANG, E. WOODRUFF and K. BROADIE, 2004 The Drosophila fragile X gene negatively regulates neuronal elaboration and synaptic differentiation. Curr. Biol. 14: 1863-1870.
41. PIRROTTA, V., 1988 Vectors for P-mediated transformation in Drosophila. Biotechnology 10: 437-456.
42. RAMOS, A., D. HOLLINGWORTH and A. PASTORE, 2003 The role of a clinically important mutation in the fold and RNA-binding properties of KH motifs. RNA 9: 293-298.
43. REEVE, S. P., L. BASSETTO, G. K. GENOVA, Y. KLEYNER, M. LEYSSEN et al., 2005 The Drosophila fragile X mental retardation protein controls actin dynamics by directly regulating profilin in the brain. Curr. Biol. 15: 1156-1163.
44. SAMBROOK, J., and D. W. RUSSELL, 2001 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. SCHAEFFER, C., B. BARDONI, J. L. MANDEL, B. EHRESMANN, C. EHRESMANN et al., 2001 The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20: 4803-4813.
46. SCHENCK, A., B. BARDONI, A. MORO, C. BAGNI and J. L. MANDEL, 2001 A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc. Natl. Acad. Sci. USA 98: 8844-8849.
47. SIOMI, H., M. C. SIOMI, R. L. NUSSBAUM and G. DREYFUSS, 1993 The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74: 291-298.
48. SIOMI, H., M. CHOI, M. C. SIOMI, R. L. NUSSBAUM and G. DREYFUSS, 1994 Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell 77: 33-39.
49. SPRADLING, A. C., and G. M. RUBIN, 1982 Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341-347.
50. VERHEIJ, C., C. E. BAKKER, E. DE GRAAFF, J. KEULEMANS, R. WILLEMSEN et al., 1993 Characterization and localization of the FMR-1 gene product associated with fragile X syndrome. Nature 363: 722-724.
51. WAN, L., T. C. DOCKENDORFF, T. A. JONGENS and G. DREYFUSS, 2000 Characterization of dFMR1, a Drosophila homolog of the fragile X mental retardation protein. Mol. Cell. Biol. 20: 8536-8547.
52. WANG, H., A. IACOANGELI, D. LIN, K. WILLIAMS, R. B. DENMAN et al., 2005 Dendritic BC1 RNA in translational control mechanisms. J. Cell Biol. 171: 811-821.
53. WASSENEGGER, M., 2005 The role of the RNAi machinery in heterochromatin formation. Cell 122: 13-16.
54. XU, K., B. A. BOGERT, W. LI, K. SU, A. LEE et al., 2004 The fragile X-related gene affects the crawling behavior of Drosophila larvae by regulating the mRNA level of the DEG/ENaC protein pickpocket1. Curr. Biol. 14: 1025-1034.
55. ZALFA, F., S. ADINOLFI, I. NAPOLI, E. KUHN-HOLSKEN, H. URLAUB et al., 2005 Fragile X mental retardation protein (FMRP) binds specifically to the brain cytoplasmic RNAs BC1/BC200 via a novel RNA-binding motif. J. Biol. Chem. 280: 33403-33410.
56. ZARNESCU, D. C., P. JIN, J. BETSCHINGER, M. NAKAMOTO, Y. WANG et al., 2005 Fragile X protein functions with lgl and the par complex in flies and mice. Dev. Cell 8: 43-52.
57. ZHANG, Y. Q., and K. BROADIE, 2005 Fathoming fragile X in fruit flies. Trends Genet. 21: 37-45.
58. ZHANG, Y., J. P. O'CONNOR, M. C. SIOMI, S. SRINIVASAN, A. DUTRA et al., 1995 The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J. 14: 5358-5366.
59. ZHANG, Y. Q., A. M. BAILEY, H. J. G. MATTHIES, R. B. RENDEN, M. A. SMITH et al., 2001 Drosophila fragile X-related gene regulates the MAP1B homolog futsch to control synaptic structure and function. Cell 107: 591-603.