NeuroMolecular Medicine

, Volume 11, Issue 3, pp 200–207 | Cite as

Macro Role(s) of MicroRNAs in Fragile X Syndrome?

Review Paper


Fragile X syndrome (FXS), the most common form of inherited mental retardation, is caused by the loss of functional fragile X mental retardation protein (FMRP). FMRP is an RNA-binding protein that can regulate the translation of specific mRNAs. It is known to regulate synaptic development through the regulation of local protein synthesis in synapses. MicroRNAs (miRNAs) are a class of small noncoding RNAs involved in almost every biological process. They exhibit spatiotemporal expression during brain development, and some miRNAs play important roles in neural development. A growing body of evidence now implicates the miRNA pathway in the molecular pathogenesis of FXS. Here we review the current state of knowledge about the microRNA pathway in neural development and the emergence of possible roles for miRNAs in FXS.


MicroRNAs Fragile X syndrome Synaptic plasticity FMRP 



We would like to thank C. Strauss for critical reading of the manuscript. This work was supported in part by NIH grant (R01 MH076090). X.L. is supported by FRAXA Postdoctoral Fellowship. P.J. is a recipient of the Beckman Young Investigator Award and the Basil O’Connor Scholar Research Award, as well as an Alfred P Sloan Research Fellow in Neuroscience.


  1. Abbott, A. L., Alvarez-Saavedra, E., Miska, E. A., Lau, N. C., Bartel, D. P., Horvitz, H. R., et al. (2005). The let-7 MicroRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Developmental Cell, 9, 403–414.CrossRefPubMedGoogle Scholar
  2. Ambros, V. (2004). The functions of animal microRNAs. Nature, 431, 350–355.CrossRefPubMedGoogle Scholar
  3. Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C., & Bassell, G. J. (2004). Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. Journal of Neuroscience, 24, 2648–2655.CrossRefPubMedGoogle Scholar
  4. Ashley, C. T., Jr., Wilkinson, K. D., Reines, D., & Warren, S. T. (1993). FMR1 protein: conserved RNP family domains and selective RNA binding. Science, 262, 563–566.CrossRefPubMedGoogle Scholar
  5. Ashraf, S. I., McLoon, A. L., Sclarsic, S. M., & Kunes, S. (2006). Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell, 124, 191–205.CrossRefPubMedGoogle Scholar
  6. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., & Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature, 455, 64–71.CrossRefPubMedGoogle Scholar
  7. Bailey, D. B., Jr., Hatton, D. D., Tassone, F., Skinner, M., & Taylor, A. K. (2001). Variability in FMRP and early development in males with fragile X syndrome. American Journal of Mental Retardation, 106, 16–27.CrossRefPubMedGoogle Scholar
  8. Baltimore, D., Boldin, M. P., O’Connell, R. M., Rao, D. S., & Taganov, K. D. (2008). MicroRNAs: new regulators of immune cell development and function. Nature Immunology, 9, 839–845.CrossRefPubMedGoogle Scholar
  9. Barbee, S. A., Estes, P. S., Cziko, A. M., Hillebrand, J., Luedeman, R. A., Coller, J. M., et al. (2006). Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron, 52, 997–1009.CrossRefPubMedGoogle Scholar
  10. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.CrossRefPubMedGoogle Scholar
  11. Bartel, D. P. (2009). MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215–233.CrossRefPubMedGoogle Scholar
  12. Bassell, G. J., & Warren, S. T. (2008). Fragile X syndrome: Loss of local mRNA regulation alters synaptic development and function. Neuron, 60, 201–214.CrossRefPubMedGoogle Scholar
  13. Berdnik, D., Fan, A. P., Potter, C. J., & Luo, L. (2008). MicroRNA processing pathway regulates olfactory neuron morphogenesis. Current Biology, 18, 1754–1759.CrossRefPubMedGoogle Scholar
  14. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., et al. (2003). Dicer is essential for mouse development. Nature Genetics, 35, 215–217.CrossRefPubMedGoogle Scholar
  15. Bolduc, F. V., Bell, K., Cox, H., Broadie, K. S., & Tully, T. (2008). Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nature Neuroscience, 11, 1143–1145.CrossRefPubMedGoogle Scholar
  16. Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B., & Cohen, S. M. (2003). Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell, 113, 25–36.CrossRefPubMedGoogle Scholar
  17. Bushati, N., & Cohen, S. M. (2008). MicroRNAs in neurodegeneration. Current Opinion in Neurobiology, 18, 292–296.CrossRefPubMedGoogle Scholar
  18. Cao, X., Yeo, G., Muotri, A. R., Kuwabara, T., & Gage, F. H. (2006). Noncoding RNAs in the mammalian central nervous system. Annual Review of Neuroscience, 29, 77–103.CrossRefPubMedGoogle Scholar
  19. Caudy, A. A., Myers, M., Hannon, G. J., & Hammond, S. M. (2002). Fragile X-related protein and VIG associate with the RNA interference machinery. Genes and Development, 16, 2491–2496.CrossRefPubMedGoogle Scholar
  20. Chang, T. C., & Mendell, J. T. (2007). microRNAs in vertebrate physiology and human disease. Annual Review of Genomics and Human Genetics, 8, 215–239.CrossRefPubMedGoogle Scholar
  21. Chang, S., Wen, S., Chen, D., & Jin, P. (2009). Small regulatory RNAs in neurodevelopmental disorders. Human Molecular Genetics, 18, R18–R26.CrossRefPubMedGoogle Scholar
  22. Choi, P. S., Zakhary, L., Choi, W. Y., Caron, S., Alvarez-Saavedra, E., Miska, E. A., et al. (2008). Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron, 57, 41–55.CrossRefPubMedGoogle Scholar
  23. Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., et al. (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proceedings of the National Academy of Sciences of the United States of America, 94, 5401–5404.CrossRefPubMedGoogle Scholar
  24. Cuellar, T. L., Davis, T. H., Nelson, P. T., Loeb, G. B., Harfe, B. D., Ullian, E., et al. (2008). Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America, 105, 5614–5619.CrossRefPubMedGoogle Scholar
  25. Cziko, A. M., McCann, C. T., Howlett, I. C., Barbee, S. A., Duncan, R. P., Luedemann, R., Zarnescu, D., Zinsmaier, K. E., Parker, R. R., Ramaswami, M. (2009). Genetic modifiers of DFMR1 encode RNA-granule components in Drosophila. Genetics, 182(4) (in press).Google Scholar
  26. Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T., et al. (2008). Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. Journal of Neuroscience, 28, 4322–4330.CrossRefPubMedGoogle Scholar
  27. De Pietri Tonelli, D., Pulvers, J. N., Haffner, C., Murchison, E. P., Hannon, G. J., & Huttner, W. B. (2008). miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development, 135, 3911–3921.CrossRefPubMedGoogle Scholar
  28. Du, T., & Zamore, P. D. (2005). microPrimer: The biogenesis and function of microRNA. Development, 132, 4645–4652.CrossRefPubMedGoogle Scholar
  29. Eichler, E. E., Richards, S., Gibbs, R. A., & Nelson, D. L. (1993). Fine structure of the human FMR1 gene. Human Molecular Genetics, 2, 1147–1153.CrossRefPubMedGoogle Scholar
  30. Feng, Y., Absher, D., Eberhart, D. E., Brown, V., Malter, H. E., & Warren, S. T. (1997a). FMRP associates with polyribosomes as an mRNP, and the I304 N mutation of severe fragile X syndrome abolishes this association. Molecular Cell, 1, 109–118.CrossRefPubMedGoogle Scholar
  31. Feng, Y., Gutekunst, C. A., Eberhart, D. E., Yi, H., Warren, S. T., & Hersch, S. M. (1997b). Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. Journal of Neuroscience, 17, 1539–1547.PubMedGoogle Scholar
  32. Ferretti, E., De Smaele, E., Miele, E., Laneve, P., Po, A., Pelloni, M., et al. (2008). Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. The EMBO Journal, 27, 2616–2627.CrossRefPubMedGoogle Scholar
  33. Fiore, R., Khudayberdiev, S., Christensen, M., Siegel, G., Flavell, S. W., Kim, T. K., et al. (2009). Mef2-mediated transcription of the miR379–410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. The EMBO Journal, 28, 697–710.CrossRefPubMedGoogle Scholar
  34. Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., et al. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science, 308, 833–838.CrossRefPubMedGoogle Scholar
  35. Goldblatt, H., Buchbinder, E., Eisikovits, Z., & Arizon-Mesinger, I. (2009). Between the professional and the private: the meaning of working with intimate partner violence in social workers’ private lives. Violence Against Women, 15, 362–384.CrossRefPubMedGoogle Scholar
  36. Grossman, A. W., Elisseou, N. M., McKinney, B. C., & Greenough, W. T. (2006). Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Brain Research, 1084, 158–164.CrossRefPubMedGoogle Scholar
  37. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature, 447, 1130–1134.CrossRefPubMedGoogle Scholar
  38. Irwin, S. A., Galvez, R., & Greenough, W. T. (2000). Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cerebral Cortex, 10, 1038–1044.CrossRefPubMedGoogle Scholar
  39. Irwin, S. A., Patel, B., Idupulapati, M., Harris, J. B., Crisostomo, R. A., Larsen, B. P., et al. (2001). Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. American Journal of Medical Genetics, 98, 161–167.CrossRefPubMedGoogle Scholar
  40. Ishizuka, A., Siomi, M. C., & Siomi, H. (2002). A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes and Development, 16, 2497–2508.CrossRefPubMedGoogle Scholar
  41. Jin, P., Alisch, R. S., & Warren, S. T. (2004a). RNA and microRNAs in fragile X mental retardation. Nature Cell Biology, 6, 1048–1053.CrossRefPubMedGoogle Scholar
  42. Jin, P., Zarnescu, D. C., Ceman, S., Nakamoto, M., Mowrey, J., Jongens, T. A., et al. (2004b). Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neuroscience, 7, 113–117.CrossRefPubMedGoogle Scholar
  43. Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., et al. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes and Development, 19, 489–501.CrossRefPubMedGoogle Scholar
  44. Kapsimali, M., Kloosterman, W. P., de Bruijn, E., Rosa, F., Plasterk, R. H., & Wilson, S. W. (2007). MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biology, 8, R173.CrossRefPubMedGoogle Scholar
  45. Karp, X., & Ambros, V. (2005). Developmental biology. Encountering microRNAs in cell fate signaling. Science, 310, 1288–1289.CrossRefPubMedGoogle Scholar
  46. Kenneson, A., Zhang, F., Hagedorn, C. H., & Warren, S. T. (2001). Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers. Human Molecular Genetics, 10, 1449–1454.CrossRefPubMedGoogle Scholar
  47. Kim, V. N., Han, J., & Siomi, M. C. (2009). Biogenesis of small RNAs in animals. Nature Reviews. Molecular Cell Biology, 10, 126–139.CrossRefPubMedGoogle Scholar
  48. Kim, J., Inoue, K., Ishii, J., Vanti, W. B., Voronov, S. V., Murchison, E., et al. (2007). A MicroRNA feedback circuit in midbrain dopamine neurons. Science, 317, 1220–1224.CrossRefPubMedGoogle Scholar
  49. Kim, D. H., Saetrom, P., Snove, O., Jr., & Rossi, J. J. (2008). MicroRNA-directed transcriptional gene silencing in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 105, 16230–16235.CrossRefPubMedGoogle Scholar
  50. Kosik, K. S. (2006). The neuronal microRNA system. Nature Reviews. Neuroscience, 7, 911–920.CrossRefPubMedGoogle Scholar
  51. Krichevsky, A. M., Sonntag, K. C., Isacson, O., & Kosik, K. S. (2006). Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells, 24, 857–864.CrossRefPubMedGoogle Scholar
  52. Laggerbauer, B., Ostareck, D., Keidel, E. M., Ostareck-Lederer, A., & Fischer, U. (2001). Evidence that fragile X mental retardation protein is a negative regulator of translation. Human Molecular Genetics, 10, 329–338.CrossRefPubMedGoogle Scholar
  53. Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.CrossRefPubMedGoogle Scholar
  54. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J., et al. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell, 117, 69–81.CrossRefPubMedGoogle Scholar
  55. Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., & Bally-Cuif, L. (2008). MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nature Neuroscience, 11, 641–648.CrossRefPubMedGoogle Scholar
  56. Li, Y., Wang, F., Lee, J. A., & Gao, F. B. (2006). MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes and Development, 20, 2793–2805.CrossRefPubMedGoogle Scholar
  57. Li, Z., Zhang, Y., Ku, L., Wilkinson, K. D., Warren, S. T., & Feng, Y. (2001). The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Research, 29, 2276–2283.CrossRefPubMedGoogle Scholar
  58. Liao, L., Park, S. K., Xu, T., Vanderklish, P., & Yates, J. R., I. I. I. (2008). Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice. Proceedings of the National Academy of Sciences of the United States of America, 105, 15281–15286.CrossRefPubMedGoogle Scholar
  59. Lugli, G., Larson, J., Martone, M. E., Jones, Y., & Smalheiser, N. R. (2005). Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. Journal of Neurochemistry, 94, 896–905.CrossRefPubMedGoogle Scholar
  60. Lugli, G., Torvik, V. I., Larson, J., & Smalheiser, N. R. (2008). Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. Journal of Neurochemistry, 106, 650–661.CrossRefPubMedGoogle Scholar
  61. Makeyev, E. V., Zhang, J., Carrasco, M. A., & Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell, 27, 435–448.CrossRefPubMedGoogle Scholar
  62. Miranda, K. C., Huynh, T., Tay, Y., Ang, Y. S., Tam, W. L., Thomson, A. M., et al. (2006). A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell, 126, 1203–1217.CrossRefPubMedGoogle Scholar
  63. Muddashetty, R. S., Kelic, S., Gross, C., Xu, M., & Bassell, G. J. (2007). Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. Journal of Neuroscience, 27, 5338–5348.CrossRefPubMedGoogle Scholar
  64. Nelson, P. T., Wang, W. X., & Rajeev, B. W. (2008). MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathology, 18, 130–138.CrossRefPubMedGoogle Scholar
  65. Nimchinsky, E. A., Oberlander, A. M., & Svoboda, K. (2001). Abnormal development of dendritic spines in FMR1 knock-out mice. Journal of Neuroscience, 21, 5139–5146.PubMedGoogle Scholar
  66. Obernosterer, G., Leuschner, P. J., Alenius, M., & Martinez, J. (2006). Post-transcriptional regulation of microRNA expression. RNA, 12, 1161–1167.CrossRefPubMedGoogle Scholar
  67. Pasquinelli, A. E., & Ruvkun, G. (2002). Control of developmental timing by micrornas and their targets. Annual Review of Cell and Developmental Biology, 18, 495–513.CrossRefPubMedGoogle Scholar
  68. Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature, 439, 283–289.CrossRefPubMedGoogle Scholar
  69. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature, 455, 58–63.CrossRefPubMedGoogle Scholar
  70. Shibata, M., Kurokawa, D., Nakao, H., Ohmura, T., & Aizawa, S. (2008). MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. Journal of Neuroscience, 28, 10415–10421.CrossRefPubMedGoogle Scholar
  71. Siegel, G., et al. (2009). A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nature Cell Biology, 11, 705–716.CrossRefPubMedGoogle Scholar
  72. Siomi, M. C., Siomi, H., Sauer, W. H., Srinivasan, S., Nussbaum, R. L., & Dreyfuss, G. (1995). FXR1, an autosomal homolog of the fragile X mental retardation gene. The EMBO Journal, 14, 2401–2408.PubMedGoogle Scholar
  73. Tay, Y., Zhang, J., Thomson, A. M., Lim, B., & Rigoutsos, I. (2008). MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature, 455, 1124–1128.CrossRefPubMedGoogle Scholar
  74. Thompson, B. J., & Cohen, S. M. (2006). The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell, 126, 767–774.CrossRefPubMedGoogle Scholar
  75. Turner, G., Webb, T., Wake, S., & Robinson, H. (1996). Prevalence of fragile X syndrome. American Journal of Medical Genetics, 64, 196–197.CrossRefPubMedGoogle Scholar
  76. Vasudevan, S., & Steitz, J. A. (2007). AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell, 128, 1105–1118.CrossRefPubMedGoogle Scholar
  77. Vasudevan, S., Tong, Y., & Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931–1934.CrossRefPubMedGoogle Scholar
  78. Verkerk, A. J., Pieretti, M., Sutcliffe, J. S., Fu, Y. H., Kuhl, D. P., Pizzuti, A., et al. (1991). Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell, 65, 905–914.CrossRefPubMedGoogle Scholar
  79. Visvanathan, J., Lee, S., Lee, B., Lee, J. W., & Lee, S. K. (2007). The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes and Development, 21, 744–749.CrossRefPubMedGoogle Scholar
  80. Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., et al. (2005). A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proceedings of the National Academy of Sciences of the United States of America, 102, 16426–16431.CrossRefPubMedGoogle Scholar
  81. Wang, W. X., Rajeev, B. W., Stromberg, A. J., Ren, N., Tang, G., Huang, Q., et al. (2008). The expression of microRNA miR-107 decreases early in Alzheimer’s disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. Journal of Neuroscience, 28, 1213–1223.CrossRefPubMedGoogle Scholar
  82. Warren, S. T., & Nelson, D. L. (1994). Advances in molecular analysis of fragile X syndrome. JAMA, 271, 536–542.CrossRefPubMedGoogle Scholar
  83. Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E., & Plasterk, R. H. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nature Genetics, 35, 217–218.CrossRefPubMedGoogle Scholar
  84. Xu, K., Bogert, B. A., Li, W., Su, K., Lee, A., & Gao, F. B. (2004). The fragile X-related gene affects the crawling behavior of Drosophila larvae by regulating the mRNA level of the DEG/ENaC protein pickpocket1. Current Biology, 14, 1025–1034.CrossRefPubMedGoogle Scholar
  85. Xu, X. L., Li, Y., Wang, F., & Gao, F. B. (2008). The steady-state level of the nervous-system-specific microRNA-124a is regulated by dFMR1 in Drosophila. Journal of Neuroscience, 28, 11883–11889.CrossRefPubMedGoogle Scholar
  86. Yang, L., Duan, R., Chen, D., Wang, J., & Jin, P. (2007). Fragile X mental retardation protein modulates the fate of germline stem cells in Drosophila. Human Molecular Genetics, 16, 1814–1820.CrossRefPubMedGoogle Scholar
  87. Zarnescu, D. C., Jin, P., Betschinger, J., Nakamoto, M., Wang, Y., Dockendorff, T. C., et al. (2005). Fragile X protein functions with lgl and the par complex in flies and mice. Developmental Cell, 8, 43–52.CrossRefPubMedGoogle Scholar
  88. Zhang, Y., O’Connor, J. P., Siomi, M. C., Srinivasan, S., Dutra, A., Nussbaum, R. L., et al. (1995). The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. The EMBO Journal, 14, 5358–5366.PubMedGoogle Scholar

Copyright information

© Humana Press Inc. 2009

Authors and Affiliations

  1. 1.Department of Human GeneticsEmory University School of MedicineAtlantaUSA

Personalised recommendations