Decreased fragile x mental retardation protein expression underlies amygdala dysfunction in carriers of the fragile x premutation

Biological Psychiatry

Volumn 70, Issue 9, 2011, Pages 859-865

  Hessl, David ^a,b   Wang, John M ^d   Schneider, Andrea ^a,b   Koldewyn, Kami ^e,f   Le, Lien ^d   Iwahashi, Christine ^c   Cheung, Katherine ^c   Tassone, Flora ^a,c   Hagerman, Paul J ^a,c   Rivera, Susan M ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Amygdala; FMR1; fragile X; FXTAS; insula; premutation

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA;

ADULT; ARTICLE; AUTISM; BASAL AMYGDALA; BRAIN FUNCTION; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CLINICAL FEATURE; COGNITION; CONTROLLED STUDY; DISEASE ASSOCIATION; EMOTIONALITY; ENZYME ACTIVITY; EYE TRACKING; FACIAL EXPRESSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE MUTATION; HUMAN; IMAGE ANALYSIS; INTELLIGENCE QUOTIENT; MALE; MOLECULAR GENETICS; NEUROPSYCHOLOGICAL TEST; ORGAN SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; TASK PERFORMANCE;

ADULT; AMYGDALA; AUTISTIC DISORDER; BRAIN; COGNITION; DNA; EMOTIONS; EYE MOVEMENTS; FRAGILE X MENTAL RETARDATION PROTEIN; HETEROZYGOTE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INTELLIGENCE TESTS; MAGNETIC RESONANCE IMAGING; MALE; MUTATION; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; RNA, MESSENGER;

EID: 80053932593     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.05.033     Document Type: Article

References (53)

1. S.L. Sherman Premature ovarian failure in the fragile X syndrome Am J Med Genet 97 2000 189 194 (Pubitemid 32059206)
2. D.J. Allingham-Hawkins, R. Babul-Hirji, D. Chitayat, J.J. Holden, K.T. Yang, and C. Lee Fragile X premutation is a significant risk factor for premature ovarian failure: The International Collaborative POF in Fragile X studypreliminary data Am J Med Genet 83 1999 322 325 (Pubitemid 29162637)
3. P.J. Hagerman, and R.J. Hagerman Fragile X-associated tremor/ataxia syndromean older face of the fragile X gene Nat Clin Pract Neurol 3 2007 107 112 (Pubitemid 46237917)
4. A. Schneider, R.J. Hagerman, and D. Hessl Fragile X syndromefrom genes to cognition Dev Disabil Res Rev 15 2009 333 342
5. I. Fernandez-Carvajal, P. Walichiewicz, X. Xiaosen, R. Pan, P.J. Hagerman, and F. Tassone Screening for expanded alleles of the FMR1 gene in blood spots from newborn males in a Spanish population J Mol Diagn 11 2009 324 329
6. C. Dombrowski, S. Levesque, M.L. Morel, P. Rouillard, K. Morgan, and F. Rousseau Premutation and intermediate-size FMR1 alleles in 10572 males from the general population: Loss of an AGG interruption is a late event in the generation of fragile X syndrome alleles Hum Mol Genet 11 2002 371 378 (Pubitemid 34213610)
7. F. Rousseau, P. Rouillard, M.L. Morel, E.W. Khandjian, and K. Morgan Prevalence of carriers of premutation-size alleles of the FMRI geneand implications for the population genetics of the fragile X syndrome Am J Hum Genet 57 1995 1006 1018
8. H. Toledano-Alhadef, L. Basel-Vanagaite, N. Magal, B. Davidov, S. Ehrlich, and V. Drasinover Fragile-X carrier screening and the prevalence of premutation and full-mutation carriers in Israel Am J Hum Genet 69 2001 351 360 (Pubitemid 32695207)
9. C.J. Moore, E.M. Daly, F. Tassone, C. Tysoe, N. Schmitz, and V. Ng The effect of pre-mutation of X chromosome CGG trinucleotide repeats on brain anatomy Brain 127 2004 2672 2681 (Pubitemid 39627376)
10. M. Aziz, E. Stathopulu, M. Callias, C. Taylor, J. Turk, and B. Oostra Clinical features of boys with fragile X premutations and intermediate alleles Am J Med Genet 121B 2003 119 127 (Pubitemid 37064041)
11. F. Farzin, H. Perry, D. Hessl, D. Loesch, J. Cohen, and S. Bacalman Autism spectrum disorders and attention-deficit/hyperactivity disorder in boys with the fragile X premutation J Dev Behav Pediatr 27 2006 S137 S144
12. B.L. Goodlin-Jones, F. Tassone, L.W. Gane, and R.J. Hagerman Autistic spectrum disorder and the fragile X premutation J Dev Behav Pediatr 25 2004 392 398
13. M. Borghgraef, J. Steyaert, S. Deroo, B. Maes, and J.P. Fryns Preliminary findings in boys with fragile X premutation: Is there a distinct behavioral phenotype? Presented at the International Fragile X Conference Washington, DC; June 2327, 2004 2004
14. J. Bourgeois, A. Seritan, E.M. Casillas, D. Hessl, A. Schneider, and Y. Yang Lifetime prevalence of mood and anxiety disorders in fragile X premutation carriers J Clin Psychiatry 72 2011 175 182
15. J.A. Bourgeois, S.M. Coffey, S.M. Rivera, D. Hessl, L.W. Gane, and F. Tassone A review of fragile X premutation disorders: Expanding the psychiatric perspective J Clin Psychiatry 70 2009 852 862
16. D. Hessl, F. Tassone, D.Z. Loesch, E. Berry-Kravis, M.A. Leehey, and L.W. Gane Abnormal elevation of FMR1 mRNA is associated with psychological symptoms in individuals with the fragile X premutation Am J Med Genet B Neuropsychiatr Genet 139 2005 115 121 (Pubitemid 41552309)
17. J.E. Roberts, D.B. Bailey Jr, J. Mankowski, A. Ford, J. Sideris, and L.A. Weisenfeld Mood and anxiety disorders in females with the FMR1 premutation Am J Med Genet B Neuropsychiatr Genet 150B 2009 130 139
18. D. Hessl, S. Rivera, K. Koldewyn, L. Cordeiro, J. Adams, and F. Tassone Amygdala dysfunction in men with the fragile X premutation Brain 130 2007 404 416 (Pubitemid 46181094)
19. D. Wechsler Wechsler Adult Intelligence ScaleThird Edition Manual 1997 The Psychological Corporation San Antonio
20. C. Lord, and M. Rutter Autism Diagnostic Observation ScheduleWPS Edition 1989 Western Psychological Services Los Angeles
21. J.N. Constantino, and R.D. Todd Intergenerational transmission of subthreshold autistic traits in the general population Biol Psychiatry 57 2005 655 660 (Pubitemid 40409704)
22. F. Tassone, R. Pan, K. Amiri, A.K. Taylor, and P.J. Hagerman A rapid polymerase chain reaction-based screening method for identification of all expanded alleles of the fragile X (FMR1) gene in newborn and high-risk populations J Mol Diagn 10 2008 43 49 (Pubitemid 351184834)
23. S. Filipovic-Sadic, S. Sah, L. Chen, J. Krosting, E. Sekinger, and W. Zhang A novel FMR1 PCR method for the routine detection of low abundance expanded alleles and full mutations in fragile X syndrome Clin Chem 56 2010 399 408
24. F. Tassone, R.J. Hagerman, A.K. Taylor, L.W. Gane, T.E. Godfrey, and P.J. Hagerman Elevated levels of FMR1 mRNA in carrier males: A new mechanism of involvement in the fragile-X syndrome Am J Hum Genet 66 2000 6 15 (Pubitemid 30481464)
25. C. Iwahashi, F. Tassone, R.J. Hagerman, D. Yasui, G. Parrott, and D. Nguyen A quantitative ELISA assay for the fragile x mental retardation 1 protein J Mol Diagn 11 2009 281 289
26. H. Zeng, and R.T. Constable Image distortion correction in EPI: Comparison of field mapping with point spread function mapping Magn Reson Med 48 2002 137 146 (Pubitemid 34721597)
27. R.A. Robb The biomedical imaging resource at Mayo Clinic IEEE Trans Med Imaging 20 2001 854 867 (Pubitemid 32992589)
28. R.A. Robb, and C. Barillot Interactive display and analysis of 3-D medical images IEEE Trans Med Imaging 8 1989 217 226 (Pubitemid 20617567)
29. R.A. Robb, D.P. Hanson, R.A. Karwoski, A.G. Larson, E.L. Workman, and M.C. Stacy Analyze: A comprehensive, operator-interactive software package for multidimensional medical image display and analysis Comput Med Imaging Graph 13 1989 433 454 (Pubitemid 20019803)
30. C.M. Schumann, J. Hamstra, B.L. Goodlin-Jones, L.J. Lotspeich, H. Kwon, and M.H. Buonocore The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages J Neurosci 24 2004 6392 6401 (Pubitemid 38944230)
31. S.M. Brown, E. Peet, S.B. Manuck, D.E. Williamson, R.E. Dahl, and R.E. Ferrell A regulatory variant of the human tryptophan hydroxylase-2 gene biases amygdala reactivity Mol Psychiatry 10 2005 805 (Pubitemid 43080111)
32. F. Ekman, and W. Friesen Pictures of Facial Affect 1976 Psychologists Press Palo Alto, CA
33. N. Tottenham, J.W. Tanaka, A.C. Leon, T. McCarry, M. Nurse, and T.A. Hare The NimStim set of facial expressions: Judgments from untrained research participants Psychiatry Res 168 2009 242 249
34. A. Bertolino, G. Arciero, V. Rubino, V. Latorre, M. De Candia, and V. Mazzola Variation of human amygdala response during threatening stimuli as a function of 5'HTTLPR genotype and personality style Biol Psychiatry 57 2005 1517 1525 (Pubitemid 40805381)
35. A.R. Hariri, V.S. Mattay, A. Tessitore, B. Kolachana, F. Fera, and D. Goldman Serotonin transporter genetic variation and the response of the human amygdala Science 297 2002 400 403 (Pubitemid 34790769)
36. K.J. Friston, A.P. Holmes, J.-P. Worsley, C.D. Poline, C.D. Frith, and R.S.J. Frackowiak Statistical parametric maps in functional imaging: A general linear approach Hum Brain Mapp 2 1995 189 210 (Pubitemid 124008664)
37. C.R. Genovese, N.A. Lazar, and T. Nichols Thresholding of statistical maps in functional neuroimaging using the false discovery rate Neuroimage 15 2002 870 878 (Pubitemid 34852500)
38. H.M. Duvernoy, and P. Bourgouin The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply 1999 Springer New York
39. A.P. Holmes, and K.J. Friston Generalisability, random effects, and population inference Hum Brain Mapp 7 1998 S754
40. M. Brett, J.L. Anton, R. Valabregue, and J.B. Pauline Region of interest analysis using an SPM toolbox Neuroimage 16 2002 S497
41. N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou, F. Crivello, O. Etard, and N. Delcroix Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain Neuroimage 15 2002 273 289 (Pubitemid 34852226)
42. A.L. Ludwig, J.W. Hershey, and P.J. Hagerman Initiation of translation of the FMR1 mRNA occurs predominantly through 5'-end-dependent ribosomal scanning J Mol Biol 407 2011 21 34
43. E.G. Allen, W. He, M. Yadav-Shah, and S.L. Sherman A study of the distributional characteristics of FMR1 transcript levels in 238 individuals Hum Genet 114 2004 439 447 (Pubitemid 38678921)
44. F. Tassone, A. Beilina, C. Carosi, S. Albertosi, C. Bagni, and L. Li Elevated FMR1 mRNA in premutation carriers is due to increased transcription RNA 13 2007 555 562 (Pubitemid 46506938)
45. A. Kenneson, F. Zhang, C.H. Hagedorn, and S.T. Warren Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers Hum Mol Genet 10 2001 1449 1454 (Pubitemid 32684886)
46. F. Tassone, R.J. Hagerman, A.K. Taylor, and P.J. Hagerman A majority of fragile X males with methylated, full mutation alleles have significant levels of FMR1 messenger RNA J Med Genet 38 2001 453 456 (Pubitemid 32661207)
47. L.S. Chen, F. Tassone, P. Sahota, and P.J. Hagerman The (CGG)n repeat element within the 5' untranslated region of the FMR1 message provides both positive and negative cis effects on in vivo translation of a downstream reporter Hum Mol Genet 12 2003 3067 3074 (Pubitemid 37508879)
48. E. Peprah, W. He, E. Allen, T. Oliver, A. Boyne, and S.L. Sherman Examination of FMR1 transcript and protein levels among 74 premutation carriers J Hum Genet 55 2010 66 68
49. D. Gothelf, J.A. Furfaro, F. Hoeft, M.A. Eckert, S.S. Hall, and R. O'Hara Neuroanatomy of fragile X syndrome is associated with aberrant behavior and the fragile X mental retardation protein (FMRP) Ann Neurol 63 2008 40 51 (Pubitemid 351240550)
50. H.C. Hazlett, M.D. Poe, A.A. Lightbody, G. Gerig, J.R. Macfall, and A.K. Ross Teasing apart the heterogeneity of autism: Same behavior, different brains in toddlers with fragile X syndrome and autism J Neurodev Disord 1 2009 81 90
51. C. Watson, F. Hoeft, A.S. Garrett, S.S. Hall, and A.L. Reiss Aberrant brain activation during gaze processing in boys with fragile X syndrome Arch Gen Psychiatry 65 2008 1315 1323
52. M.F. Bear Therapeutic implications of the mGluR theory of fragile X mental retardation Genes Brain Behav 4 2005 393 398 (Pubitemid 41192450)
53. G. Dolen, E. Osterweil, B.S. Rao, G.B. Smith, B.D. Auerbach, and S. Chattarji Correction of fragile X syndrome in mice Neuron 56 2007 955 962 (Pubitemid 350251119)