Matrix metalloproteinase-deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome

Neurobiology of Disease

Volumn 89, Issue , 2016, Pages 126-135

  Lovelace, Jonathan W ^a   Wen, Teresa H ^a   Reinhard, Sarah ^a   Hsu, Mike S ^b   Sidhu, Harpreet ^a,b   Ethell, Iryna M ^a,b   Binder, Devin K ^a,b   Razak, Khaleel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Auditory cortex; Autism; Cortical event related potentials; Fragile X Syndrome; Matrix metalloproteinase 9; Sensory hypersensitivity

Indexed keywords

GELATINASE B; FMR1 PROTEIN, MOUSE; FRAGILE X MENTAL RETARDATION PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; EVENT RELATED POTENTIAL; EVOKED AUDITORY RESPONSE; FRAGILE X SYNDROME; HABITUATION; LATENT PERIOD; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; WILD TYPE; ADAPTATION; ANIMAL; AUDITORY EVOKED POTENTIAL; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; UPREGULATION;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY CORTEX; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; UP-REGULATION;

EID: 84957950220     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.02.002     Document Type: Article

References (44)

1. Bailey D.B., Mesibov G.B., Hatton D.D., Clark R.D., Roberts J.E., Mayhew L. Autistic behavior in young boys with fragile X syndrome. J. Autism Dev. Disord. 1998, 28:499-508.
2. Bilousova T.V., Dansie L., Ngo M., Aye J., Charles J.R., Ethell D.W., Ethell I.M. Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J. Med. Genet. 2009, 46(2):94-102.
3. Cabungcal J.H., Steullet P., Morishita H., Kraftsik R., Cuenod M., Hensch T.K., Do K.Q. Perineuronal nets protect fast-spiking interneurons against oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:9130-9135.
4. Castren M., Paakkonen A., Tarkka I.M., Ryynanen M., Partanen J. Augmentation of auditory N1 in children with fragile X syndrome. Brain Topogr. 2003, 15:165-171.
5. Chen L., Toth M. Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 2001, 103:1043-1050.
6. Deng P.Y., Rotman Z., Blundon J.A., Cho Y., Cui J., Cavalli V., Zakharenko S.S., Klyachko V.A. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 2013, 77(4):696-711.
7. Dziembowska M., Pretto D.I., Janusz A., Kaczmarek L., Leigh M.J., Gabriel N., Durbin-Johnson B., Hagerman R.J., Tassone F. High MMP-activity levels in fragile X syndrome are lowered by minocycline. Am. J. Med. Genet. Part A 2013, 161(8):1897-1903.
8. Ethell I.M., Ethell D.W. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J. Neurosci. Res. 2007, 85(13):2813-2823.
9. Fruhstorfer H., Soveri P., Järvilehto T. Short-term habituation of the auditory evoked response in man. Electroen. Clin. Neuro. 1970, 28(2):153-161.
10. Gibson J.R., Bartley A.F., Hays S.A., Huber K.M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 2008, 100:2615-2626.
11. Gkogkas C.G., Khoutorsky A., Cao R., Jafarnejad S.M., Prager-Khoutorsky M., Giannakas N., Kaminari A., Fragkouli A., Nader K., Price T.J., Konicek B.W., Graff J.R., Tzinia A.K., Lacaille J.C., Sonenberg N. Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes. Cell Rep. 2014, 9:1742-1755.
12. Green S.A., Hernandez L., Tottenham N., Krasileva K., Bookheimer S.Y., Dapretto M. Neurobiology of sensory overresponsivity in youth with autism spectrum disorders. JAMA Psychiatry 2015, 10.1001/jamapsychiatry.2015.0737.
13. Hagerman R.J., Hagerman P. Advances in clinical and molecular understanding of the FMR1 premutation and fragile X-associated tremor/ataxia syndrome. Lancet Neurol. 2013, 12(8):786-798.
14. Hagerman R.J., Jackson A.W., Levitas A., Rimland B., Braden M. An analysis of autism in fifty males with the fragile X syndrome. Am. J. Med. Genet. 1986, 23:359-374.
15. Hagerman R.J., Amiri K., Cronister A. Fragile X checklist. Am. J. Med. Genet. 1991, 38:283-287.
16. Janusz A., Miłek J., Perycz M., Pacini L., Bagni C., Kaczmarek L., Dziembowska M. The fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses. J. Neurosci. 2013, 33(46):18234-18241.
17. Kaliszewska A., Bijata M., Kaczmarek L., Kossut M. Experience-dependent plasticity of the barrel cortex in mice observed with 2-DG brain mapping and c-Fos: effects of MMP-KO. Cereb. Cortex 2012, 22:2160-2170.
18. Karhu J., Herrgård E., Luoma L., Airaksinen E., Partanen J. Dual cerebral processing of elementary auditory input in children. Neuroreport 1997, 8(6):1327-1330.
19. Lai M.C., Lombardo M.V., Baron-Cohen S. Autism. Lancet 2014, 83(9920):896-910.
20. Lee C.Z., Yao J.S., Huang Y., Zhai W., Liu W., Guglielmo B.J., Lin E., Yang G.Y., Young W.L. Dose-response effect of tetracyclines on cerebral matrix metalloproteinase-after vascular endothelial growth factor hyperstimulation. J. Cereb. Blood Flow Metab. 2006, 26(9):1157-1164.
21. Martin del Campo H., Measor K., Razak K.A. Parvalbumin immunoreactivity in the auditory cortex of a mouse model of presbycusis. Hear. Res. 2012, 294:31-39.
22. Mouraux A., Iannetti G.D. Across-trial averaging of event-related EEG responses and beyond. Magn. Reson. Imaging 2008, 26:1041-1054.
23. Musumeci S.A., Calabrese G., Bonaccorso C.M., D'Antoni S., Brouwer J.R., Bakker C.E., Elia M., Ferri R., Nelson D.L., Oostra B.A., Catania M.V. Audiogenic seizure susceptibility is reduced in fragile X knockout mice after introduction of FMR1 transgenes. Exp. Neurol. 2007, 203:233-240.
24. O'Donnell W.T., Warren S.T. A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 2002, 25:315-338.
25. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2004, Gulf Professional Publishing, Houston, TX.
26. Reinhard S.M., Razak K., Ethell I.M. A delicate balance: role of MMP-in brain development and pathophysiology of neurodevelopmental disorders. Front. Cell. Neurosci. 2015, 9:280. 10.3389/fncel.2015.00280.
27. Roberts J., Price J., Barnes E., Nelson L., Burchinal M., Hennon E.A., Moskowitz L., Edwards A., Malkin C., Anderson K., Misenheimer J., Hooper S.R. Receptive vocabulary, expressive vocabulary, and speech production of boys with fragile X syndrome in comparison to boys with down syndrome. Am. J. Ment. Retard. 2007, 177-193.
28. Rosburg T., Trautner P., Korzyukov O.A., Boutros N.N., Schaller C., Elger C.E., Kurthen M. Short-term habituation of the intracranially recorded auditory evoked potentials P50 and N100. Neurosci. Lett. 2004, 372:245-249.
29. Rotschafer S.E., Razak K.A. Altered auditory processing in a mouse model of fragile X syndrome. Brain Res. 2013, 1506:12-24.
30. Rotschafer S.E., Razak K.A. Auditory processing in fragile x syndrome. Front. Cell. Neurosci. 2014, 8:19.
31. Rotschafer S.E., Marshak S., Cramer K.S. Deletion of Fmr1 alters function and synaptic inputs in the auditory brainstem. PLoS ONE 2015, 10(2). 10.1371/journal.pone.0117266.
32. Schneider A., Leigh M.J., Adams P., Nanakul R., Chechi T., Olichney J., Hagerman R., Hessl D. Electrocortical changes associated with minocycline treatment in fragile X syndrome. J. Psychopharmacol. 2013, 27:956-963.
33. Selby L., Zhang C., Sun Q.Q. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci. Lett. 2007, 412(3):227-232.
34. Sherman SL (2002) Epidimiology. In: Fragile X Syndrome: Diagnosis, Treatment, and Research (Hagerman RJ, Hagerman PJ, ed), pp 136-168. Baltimore: Johns Hopkins UP.
35. Sidhu H., Dansie L.E., Hickmott P.W., Ethell D.W., Ethell I.M. Genetic removal of matrix metalloproteinase 9 rescues the symptoms of fragile X syndrome in a mouse model. J. Neurosci. 2014, 34:9867-9879.
36. St Clair D.M., Blackwood D.H., Oliver C.J., Dickens P. P3 abnormality in fragile X syndrome. Biol. Psychiatry 1987, 22:303-312.
37. Strumbos J.G., Brown M.R., Kronengold J., Polley D.B., Kaczmarek L.K. Fragile X mental retardation protein is required for rapid experience-dependent regulation of the potassium channel Kv3.1b. J. Neurosci. 2010, 30:10263-10271.
38. Van der Molen M.J., Van der Molen M.W., Ridderinkhof K.R., Hamel B.C., Curfs L.M., Ramakers G.J. Auditory change detection in fragile X syndrome males: a brain potential study. Clin. Neurophysiol. 2012, 123:1309-1318.
39. Van der Molen M.J., Van der Molen M.W., Ridderinkhof K.R., Hamel B.C., Curfs L.M., Ramakers G.J. Auditory and visual cortical activity during selective attention in fragile X syndrome: a cascade of processing deficiencies. J. Clin. Neurophysiol. 2012, 123:720-729.
40. Wang J., Caspary D., Salvi R.J. GABA-antagonist causes dramatic expansion of tuning in primary auditory cortex. Neuroreport 2000, 11:1137-1140.
41. Wang Y., Sakano H., Beebe K., Brown M.R., de Laat R., Bothwell M., Kulesza R.J., Rubel E.W. Intense and specialized dendritic localization of the fragile X mental retardation protein in binaural brainstem neurons: a comparative study in the alligator, chicken, gerbil, and human. J. Comp. Neurol. 2014, 522:2107-2128.
42. Wehr M., Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446.
43. Wu G.K., Arbuckle R., Liu B.H., Tao H.W., Zhang L.I. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 2008, 58:132-143.
44. Yu T.W., Berry-Kravis E. Autism and fragile X syndrome. Semin. Neurol. 2014, 34(3):258-265.