Systematic mapping of fragile X granules in the mouse brain reveals a potential role for presynaptic FMRP in sensorimotor functions

Journal of Comparative Neurology

Volumn 520, Issue 16, 2012, Pages 3687-3706

  Akins, Michael R ^a   Leblanc, Hannah F ^a   Stackpole, Emily E ^a   Chyung, Eunice ^a   Fallon, Justin R ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Axonal protein synthesis; Local translation; RNA binding proteins

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL TISSUE; ANTERIOR COMMISSURE; ARTICLE; BRAIN CELL; BRAIN MAPPING; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; FRAGILE X GRANULE; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NERVE FIBER; NEUROMODULATION; NONHUMAN; OLFACTORY BULB; POSITIVE FEEDBACK; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORIMOTOR FUNCTION; THALAMOCORTICAL TRACT; THALAMUS NUCLEUS; THALAMUS RETICULAR NUCLEUS;

ANIMALS; BLOTTING, WESTERN; BRAIN; CYTOPLASMIC GRANULES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PRESYNAPTIC TERMINALS;

EID: 84865848777     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23123     Document Type: Article

References (48)

1. Akins MR, Greer CA. 2006. Cytoskeletal organization of the developing mouse olfactory nerve layer. J Comp Neurol 494: 358-367.
2. Akins MR, Berk-Rauch HE, Fallon JR. 2009. Presynaptic translation: stepping out of the postsynaptic shadow. Front Neural Circuits 3: 17.
3. Baranek GT, Roberts JE, David FJ, Sideris J, Mirrett PL, Hatton DD, Bailey DBJr. 2008. Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Phys Occup Ther Pediatr 28: 79-98.
4. Bassell GJ, Warren ST. 2008. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60: 201-214.
5. Bontekoe CJM, McIlwain KL, Nieuwenhuizen IM, Yuva-Paylor LA, Nellis A, Willemsen R, Fang Z, Kirkpatrick L, Bakker CE, McAninch R, et al. 2002. Knockout mouse model for Fxr2: a model for mental retardation. Hum Mol Genet 11: 487-498.
6. Brown MR, Kronengold J, Gazula V-R, Chen Y, Strumbos JG, Sigworth FJ, Navaratnam D, Kaczmarek LK. 2010. Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat Neurosci 13: 819-821.
7. Chen L, Toth M. 2001. Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 103: 1043-1050.
8. Christie SB, Akins MR, Schwob JE, Fallon JR. 2009. The FXG: a presynaptic Fragile X granule expressed in a subset of developing brain circuits. J Neurosci 29: 1514-1524.
9. Cohen D, Pichard N, Tordjman S, Baumann C, Burglen L, Excoffier E, Lazar G, Mazet P, Pinquier C, Verloes A, et al. 2005. Specific genetic disorders and autism: clinical contribution towards their identification. J Autism Dev Disord 35: 103-116.
10. Cook D, del Rayo Sanchez-Carbente M, Lachance C, Radzioch D, Tremblay S, Khandjian EW, DesGroseillers L, Murai KK. 2011. Fragile X related protein 1 clusters with ribosomes and messenger RNAs at a subset of dendritic spines in the mouse hippocampus. PLoS ONE 6: e26120.
11. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N. 2009. Translational control of long-lasting synaptic plasticity and memory. Neuron 61: 10-26.
12. Cuschieri A, Bannister LH. 1975. Development of olfactory mucosa in mouse-electron-microscopy. J Anat 119: 471-498.
13. Darnell JC, Van Driesche SJ, Zhang C, Hung KYS, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, et al. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146: 247-261.
14. Davis BJ, Macrides F. 1981. The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment, and piriform cortex to the main olfactory bulb in the hamster: an autoradiographic study. J Comp Neurol 203: 475-493.
15. Deng P-Y, Sojka D, Klyachko VA. 2011. Abnormal presynaptic short-term plasticity and information processing in a mouse model of Fragile X syndrome. J Neurosci 31: 10971-10982.
16. Gabel LA, Won S, Kawai H, McKinney M, Tartakoff AM, Fallon JR. 2004. Visual experience regulates transient expression and dendritic localization of Fragile X mental retardation protein. J Neurosci 24: 10579-10583.
17. Garnon J, Lachance C, Di Marco S, Hel Z, Marion D, Ruiz MC, Newkirk MM, Khandjian EW, Radzioch D. 2005. Fragile X-related protein FXR1P regulates proinflammatory cytokine tumor necrosis factor expression at the post-transcriptional level. J Biol Chem 280: 5750-5763.
18. Gatto CL, Broadie K. 2008. Temporal requirements of the Fragile X mental retardation protein in the regulation of synaptic structure. Development 135: 2637-2648.
19. Giuditta A, Tai Chun J, Eyman M, Cefaliello C, Bruno AP, Crispino M. 2008. Local gene expression in axons and nerve endings: the glia-neuron unit. Physiol Rev 88: 515-555.
20. Hanson JE, Madison DV. 2007. Presynaptic Fmr1 genotype influences the degree of synaptic connectivity in a mosaic mouse model of Fragile X syndrome. J Neurosci 27: 4014-4018.
21. He X-P, Kotloski R, Nef S, Luikart BW, Parada LF, McNamara JO. 2004. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43: 31-42.
22. Hernandez RN, Feinberg RL, Vaurio R, Passanante NM, Thompson RE, Kaufmann WE. 2009. Autism spectrum disorder in fragile X syndrome: A longitudinal evaluation. Am J Med Genet A 149A: 1125-1137.
23. Hinds JW, Hinds PL. 1976. Synapse formation in the mouse olfactory bulb. Quantitative studies. J Comp Neurol 169: 15-40.
24. Hoeft F, Carter JC, Lightbody AA, Cody Hazlett H, Piven J, Reiss AL. 2010. Region-specific alterations in brain development in one- to three-year-old boys with Fragile X syndrome. Proc Natl Acad Sci U S A 107: 9335-9339.
25. Ishizuka N, Weber J, Amaral DG. 1990. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295: 580-623.
26. Jones EG. 1975. Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162: 285-308.
27. Kakei S, Na J, Shinoda Y. 2001. Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J Comp Neurol 437: 170-185.
28. Kau ASM, Meyer WA, Kaufmann WE. 2002. Early development in males with Fragile X syndrome: A review of the literature. Microsc Res Tech 57: 174-178.
29. Largo RH, Schinzel A. 1985. Developmental and behavioural disturbances in 13 boys with fragile X syndrome. Eur J Pediatr 143: 269-275.
30. Lorente de No R. 1934. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46: 113-177.
31. Mason P. 2001. Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Annu Rev Neurosci 24: 737-777.
32. Mientjes EJ, Nieuwenhuizen I, Kirkpatrick L, Zu T, Hoogeveen-Westerveld M, Severijnen L, Rifé M, Willemsen R, Nelson DL, Oostra BA. 2006. The generation of a conditional Fmr1 knock out mouse model to study Fmrp function in vivo. Neurobiol Dis 21: 549-555.
33. Miller LJ, McIntosh DN, McGrath J, Shyu V, Lampe M, Taylor AK, Tassone F, Neitzel K, Stackhouse T, Hagerman RJ. 1999. Electrodermal responses to sensory stimuli in individuals with Fragile X syndrome: a preliminary report. Am J Med Genet 83: 268-279.
34. Pacey LKK, Doering LC. 2007. Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Glia 55: 1601-1609.
35. Paxinos G, Franklin KBJ. 2007. The mouse brain in stereotaxic coordinates, 3rd ed. New York: Academic Press.
36. Pickett J, London E. 2005. The neuropathology of autism: a review. J Neuropathol Exp Neurol 64: 925-935.
37. Price TJ, Flores CM, Cervero F, Hargreaves KM. 2006. The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons. Neuroscience 141: 2107-2116.
38. Roberts JE, Mankowski JB, Sideris J, Goldman BD, Hatton DD, Mirrett PL, Baranek GT, Reznick JS, Long ACJ, Bailey DB. 2009. Trajectories and predictors of the development of very young boys with Fragile X syndrome. J Pediatr Psychol 34: 827-836.
39. Roy S, Zhao Y, Allensworth M, Farook MF, LeDoux MS, Reiter LT, Heck DH. 2011. Comprehensive motor testing in Fmr1-KO mice exposes temporal defects in oromotor coordination. Behav Neurosci 125: 962-969.
40. Stepniewska I, Preuss TM, Kaas JH. 1994. Thalamic connections of the primary motor cortex (M1) of owl monkeys. J Comp Neurol 349: 558-582.
41. Swanson LW, Wyss JM, Cowan WM. 1978. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181: 681-715.
42. Till SM, Li H-L, Miniaci MC, Kandel ER, Choi Y-B. 2011. A presynaptic role for FMRP during protein synthesis-dependent long-term plasticity in Aplysia. Learn Mem 18: 39-48.
43. Till SM, Wijetunge LS, Seidel VG, Harlow E, Wright AK, Bagni C, Contractor A, Gillingwater TH, Kind PC. 2012. Altered maturation of the primary somatosensory cortex in a mouse model of Fragile X syndrome. Hum Mol Genet 21: 2143-2156.
44. Zang JB, Nosyreva ED, Spencer CM, Volk LJ, Musunuru K, Zhong R, Stone EF, Yuva-Paylor LA, Huber KM, Paylor R, et al. 2009. A mouse model of the human Fragile X syndrome I304N mutation. PLoS Genet 5: e1000758.
45. Zhang YQ, Bailey AM, Matthies HJG, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K. 2001. Drosophila Fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107: 591-603.
46. Zhang J, Hou L, Klann E, Nelson DL. 2009. Altered hippocampal synaptic plasticity in the Fmr1 gene family knockout mouse models. J Neurophysiol 101: 2572-2580.
47. Zingerevich C, Greiss-Hess L, Lemons-Chitwood K, Harris SW, Hessl D, Cook K, Hagerman RJ. 2009. Motor abilities of children diagnosed with Fragile X syndrome with and without autism. J Intellect Disabil Res 53: 11-18.
48. Zukin RS, Richter JD, Bagni C. 2009. Signals, synapses, and synthesis: how new proteins control plasticity. Front Neural Circuits 3: 14.