Long-lasting effects of minocycline on behavior in young but not adult Fragile X mice

Neuroscience

Volumn 246, Issue , 2013, Pages 186-198

  Dansie, L E ^a   Phommahaxay, K ^a   Okusanya, A G ^a   Uwadia, J ^a   Huang, M ^a   Rotschafer, S E ^b   Razak, K A ^b   Ethell, D W ^c   Ethell, I M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

Anxiety; Audiogenic seizures; Fragile X Syndrome; Hyperactivity; Minocycline; Perseverance

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN G; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE B BETA;

AGE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDIOGENIC SEIZURE; BEHAVIOR CHANGE; CONTROLLED STUDY; DISEASE CONTROL; DISEASE MODEL; ENZYME ACTIVATION; EXPERIMENTAL TEST; FRAGILE X SYNDROME; KNOCKOUT MOUSE; LOCOMOTION; MALE; MARBLE BURYING TEST; MAZE TEST; MOUSE; NEWBORN; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; TRANQUILIZING ACTIVITY; TREATMENT DURATION;

EID: 84878921815     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.04.058     Document Type: Article

References (75)

1. Banko J.L., Hou L., Poulin F., Sonenberg N., Klann E. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2006, 26:2167-2173.
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, 46:94-102.
3. Bozdagi O., Nagy V., Kwei K.T., Huntley G.W. In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J Neurophysiol 2007, 98:334-344.
4. Brown V., Small K., Lakkis L., Feng Y., Gunter C., Wilkinson K.D., Warren S.T. Purified recombinant Fmrp exhibits selective RNA binding as an intrinsic property of the Fragile X mental retardation protein. J Biol Chem 1998, 273:15521-15527.
5. Brown R.E., Corey S.C., Moore A.K. Differences in measures of exploration and fear in MHC-congenic C57BL/6J and B6-H-2K mice. Behav Genet 1999, 29:263-271.
6. Bruno M.A., Mufson E.J., Wuu J., Cuello A.C. Increased matrix metalloproteinase 9 activity in mild cognitive impairment. J Neuropathol Exp Neurol 2009, 68:1309-1318.
7. Carlisle H.J., Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci 2005, 28:182-187.
8. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
9. Corley RB (2004) Antibodies. In: Immunology, infection, and immunity: An introductory text (Pier, G. B. et al., eds), pp 113-143 Washington, DC: ASM Press.
10. Darnell J.C., Van Driesche S.J., Zhang C., Hung K.Y., Mele A., Fraser C.E., Stone E.F., Chen C., Fak J.J., Chi S.W., Licatalosi D.D., Richter J.D., Darnell R.B. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 2011, 146:247-261.
11. Dolen G., Osterweil E., Rao B.S., Smith G.B., Auerbach B.D., Chattarji S., Bear M.F. Correction of Fragile X syndrome in mice. Neuron 2007, 56:955-962.
12. Dziembowska M., Milek J., Janusz A., Rejmak E., Romanowska E., Gorkiewicz T., Tiron A., Bramham C.R., Kaczmarek L. Activity-dependent local translation of matrix metalloproteinase-9. J Neurosci 2012, 32:14538-14547.
13. Dziembowska M, Pretto DI, Janusz A, Kaczmarek L, Leigh MJ, Gabriel N, Durbin-Johnson B, Hagerman RJ, Tassone F (in press) High activity levels of MMP-9 in Fragile X syndrome are lowered by minocycline. Am J Med Gen.
14. Elkayam O., Yaron M., Caspi D. Minocycline-induced autoimmune syndromes: an overview. Semin Arthritis Rheum 1999, 28:392-397.
15. Ethell I.M., Pasquale E.B. Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 2005, 75:161-205.
16. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res Brain Res Rev 2002, 39:29-54.
17. Gallagher S.M., Daly C.A., Bear M.F., Huber K.M. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci 2004, 24:4859-4864.
18. Garattini S., Valzelli L. Is the isolated animal a possible model for phobia and anxiety?. Prog Neuropsychopharmacol 1981, 5:159-165.
19. Greenough W.T., Klintsova A.Y., Irwin S.A., Galvez R., Bates K.E., Weiler I.J. Synaptic regulation of protein synthesis and the Fragile X protein. PNAS 2001, 98:7101-7106.
20. Grossman A.W., Aldridge G.M., Weiler I.J., Greenough W.T. Local protein synthesis and spine morphogenesis: Fragile X syndrome and beyond. J Neurosci 2006, 26:7151-7155.
21. Gyertyan I. Analysis of the marble burying response: marbles serve to measure digging rather than evoke burying. Behav Pharmacol 1995, 6:24-31.
22. Hagerman R., Hagerman P. The physical and behavioral phenotype. Syndrome: diagnosis, treatment, and research 2002, 3-109. The Johns Hopkins University Press, Baltimore. X. Fragile (Ed.).
23. Hagerman R., Hoem G., Hagerman P. Fragile X and autism: intertwined at the molecular level leading to targeted treatments. Mol Autism 2010, 1:12.
24. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 1999, 9:343-348.
25. Hashimoto K., Ishima T. A novel target of action of minocycline in NGF-induced neurite outgrowth in PC12 cells: translation initiation [corrected] factor eIF4AI. PLoS One 2010, 5:e15430.
26. Hou L., Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2004, 24:6352-6361.
27. Hou L., Antion M.D., Hu D., Spencer C.M., Paylor R., Klann E. Dynamic translational and proteasomal regulation of Fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 2006, 51:441-454.
28. Kaufmann W.E., Moser H.W. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000, 10:981-991.
29. Khandjian E.W. Biology of the Fragile X mental retardation protein, an RNA-binding protein. Biochem Cell Biol 1999, 77:331-342.
30. Kim S.H., Markham J.A., Weiler I.J., Greenough W.T. Aberrant early-phase ERK inactivation impedes neuronal function in Fragile X syndrome. PNAS 2008, 105:4429-4434.
31. Lawson T.M., Amos N., Bulgen D., Williams B.D. Minocycline-induced lupus: clinical features and response to rechallenge. Rheumatology (Oxford) 2001, 40:329-335.
32. 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-9 after vascular endothelial growth factor hyperstimulation. J Cereb Blood Flow Metab 2006, 26:1157-1164.
33. Leigh M.J., Nguyen D.V., Mu Y., Winarni T.I., Schneider A., Checi T., Polussa J., Doucet P., Tassone F., Rivera S., Hessl D., Hagerman R.J. A randomized double-blind, placebo-controlled trial of minocycline in children and adolescents with Fragile X sydrome. J Dev Behav Pediatr 2013, 34:147-155.
34. Lin S., Wei X., Bales K.R., Paul A.B., Ma Z., Yan G., Paul S.M., Du Y. Minocycline blocks bilirubin neurotoxicity and prevents hyperbilirubinemia-induced cerebellar hypoplasia in the Gunn rat. Eur J Neurosci 2005, 22:21-27.
35. Luzi P., Abraham R.M., Rafi M.A., Curtis M., Hooper D.C., Wenger D.A. Effects of treatments on inflammatory and apoptotic markers in the CNS of mice with globoid cell leukodystrophy. Brain Res 2009, 1300:146-158.
36. Michaluk P., Wawrzyniak M., Alot P., Szczot M., Wyrembek P., Mercik K., Medvedev N., Wilczek E., De Roo M., Zuschratter W., Muller D., Wilczynski G.M., Mozrzymas J.W., Stewart M.G., Kaczmarek L., Wlodarczyk J. Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J Cell Sci 2011, 124:3369-3380.
37. Min W.W., Yuskaitis C.J., Yan Q., Sikorski C., Chen S., Jope R.S., Bauchwitz R.P. Elevated glycogen synthase kinase-3 activity in Fragile X mice: key metabolic regulator with evidence for treatment potential. Neuropharmacology 2009, 56:463-472.
38. Mines M.A., Yuskaitis C.J., King M.K., Beurel E., Jope R.S. GSK3 influences social preference and anxiety-related behaviors during social interaction in a mouse model of Fragile X syndrome and autism. PLoS One 2010, 5:e9706.
39. Musumeci S.A., Hagerman R.J., Ferri R., Bosco P., Dalla Bernardina B., Tassinari C.A., De Sarro G.B., Elia M. Epilepsy and EEG findings in males with Fragile X syndrome. Epilepsia 1999, 40:1092-1099.
40. Musumeci S.A., Bosco P., Calabrese G., Bakker C., De Sarro G.B., Elia M., Ferri R., Oostra B.A. Audiogenic seizures susceptibility in transgenic mice with Fragile X syndrome. Epilepsia 2000, 41:19-23.
41. Nagy V., Bozdagi O., Matynia A., Balcerzyk M., Okulski P., Dzwonek J., Costa R.M., Silva A.J., Kaczmarek L., Huntley G.W. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 2006, 26:1923-1934.
42. Nagy V., Bozdagi O., Huntley G.W. The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory. Learn Mem 2007, 14:655-664.
43. Narayanan U., Nalavadi V., Nakamoto M., Pallas D.C., Ceman S., Bassell G.J., Warren S.T. FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 2007, 27:14349-14357.
44. Njung'e K., Handley S.L. Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav 1991, 38:63-67.
45. Okulski P., Jay T.M., Jaworski J., Duniec K., Dzwonek J., Konopacki F.A., Wilczynski G.M., Sánchez-Capelo A., Mallet J., Kaczmarek L. TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol Psychiatry 2007, 62:359-362.
46. Pan D., Sciascia A., Vorhees C.V., Williams M.T. Progression of multiple behavioral deficits with various ages of onset in a murine model of Hurler syndrome. Brain Res 2008, 1188:241-253.
47. Paribello C., Tao L., Folino A., Berry-Kravis E., Tranfaglia M., Ethell I.M., Ethell D.W. Open-label add-on treatment trial of minocycline in Fragile X syndrome. BMC Neurol 2010, 10:91.
48. Peineau S., Bradley C., Taghibiglou C., Doherty A., Bortolotto Z.A., Wang Y.T., Collingridge G.L. The role of GSK-3 in synaptic plasticity. Br J Pharmacol 2008, 153(Suppl. 1):S428-S437.
49. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 1986, 24:525-529.
50. Pfeiffer B.E., Huber K.M. The state of synapses in Fragile X syndrome. Neuroscientist 2009, 15:549-567.
51. Pi R., Li W., Lee N.T., Chan H.H., Pu Y., Chan L.N., Sucher N.J., Chang D.C., Li M., Han Y. Minocycline prevents glutamate-induced apoptosis of cerebellar granule neurons by differential regulation of p38 and Akt pathways. J Neurochem 2004, 91:1219-1230.
52. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
53. Qin M., Smith C.B. Unaltered hormonal response to stress in a mouse model of Fragile X syndrome. Psychoneuroendocrinology 2008, 33:883-889.
54. Romero-Zerbo Y., Decara J., el Bekay R., Sanchez-Salido L., Del Arco-Herrera I., de Fonseca F.R., de Diego-Otero Y. Protective effects of melatonin against oxidative stress in Fmr1 knockout mice: a therapeutic research model for the Fragile X syndrome. J Pineal Res 2009, 46:224-234.
55. Rotschafer S.E., Trujillo M.S., Dansie L.E., Ethell I.M., Razak K.A. Minocycline treatment reverses ultrasonic vocalization production deficit in a mouse model of Fragile X Syndrome. Brain Res 2012, 1439:7-14.
56. Rudelli R.D., Brown W.T., Wisniewski K., Jenkins E.C., Laure-Kamionowska M., Connell F., Wisniewski H.M. Adult Fragile X syndrome. Clinico-neuropathologic findings. Acta Neuropathol 1985, 67:289-295.
57. Sharma A., Hoeffer C.A., Takayasu Y., Miyawaki T., McBride S.M., Klann E., Zukin R.S. Dysregulation of mTOR signaling in Fragile X syndrome. J Neurosci 2010, 30:694-702.
58. Siller S.S., Broadie K. Neural circuit architecture defects in a Drosophila model of Fragile X syndrome are alleviated by minocycline treatment and genetic removal of matrix metalloproteinase. Dis Model Mech 2011, 4:673-685.
59. Siller S.S., Broadie K. Matrix metalloproteinases and minocycline: therapeutic avenues for Fragile X syndrome. Neural Plast 2012, 2012:124548.
60. Simon P., Panissaud C., Costentin J. The stimulant effect of modafinil on wakefulness is not associated with an increase in anxiety in mice. A comparison with dexamphetamine. Psychopharmacology (Berl) 1994, 114:597-600.
61. Spencer C.M., Alekseyenko O., Hamilton S.M., Thomas A.M., Serysheva E., Yuva-Paylor L.A., Paylor R. Modifying behavioral phenotypes in Fmr1KO mice: genetic background differences reveal autistic-like responses. Autism Res 2011, 4:40-56.
62. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology 2009, 204:361-373.
63. Utari A., Chonchaiya W., Rivera S.M., Schneider A., Hagerman R.J., Faradz S.M., Ethell I.M., Nguyen D.V. Side effects of minocycline treatment in patients with Fragile X syndrome and exploration of outcome measures. Am J Intellect Dev Disabil 2010, 115:433-443.
64. Valzelli L. The "isolation syndrome" in mice. Psychopharmacologia 1973, 31:305-320.
65. Voikar V., Polus A., Vasar E., Rauvala H. Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav 2005, 4:240-252.
66. X-b Wang., Bozdagi O., Nikitczuk J.S., Zhai Z.W., Zhou Q., Huntley G.W. Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. PNAS 2008, 105:19520-19525.
67. Wilczynski G.M., Konopacki F.A., Wilczek E., Lasiecka Z., Gorlewicz A., Michaluk P., Wawrzyniak M., Malinowska M., Okulski P., Kolodziej L.R., Konopka W., Duniec K., Mioduszewska B., Nikolaev E., Walczak A., Owczarek D., Gorecki D.C., Zuschratter W., Ottersen O.P., Kaczmarek L. Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol 2008, 180:1021-1035.
68. Wilkins A., Nikodemova M., Compston A., Duncan I. Minocycline attenuates nitric oxide-mediated neuronal and axonal destruction in vitro. Neuron Glia Biol 2004, 1:297-305.
69. Winarni T.I., Schneider A., Borodyanskara M., Hagerman R.J. Early intervention combined with targeted treatment promotes cognitive and behavioral improvements in young children with Fragile X syndrome. Case Rep Genet 2012, 2012:4.
70. Yan Q.J., Asafo-Adjei P.K., Arnold H.M., Brown R.E., Bauchwitz R.P. A phenotypic and molecular characterization of the fmr1-tm1Cgr Fragile X mouse. Genes Brain Behav 2004, 3:337-359.
71. Yan Q.J., Rammal M., Tranfaglia M., Bauchwitz R.P. Suppression of two major Fragile X Syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 2005, 49:1053-1066.
72. Yao J.S., Chen Y., Zhai W., Xu K., Young W.L., Yang G.Y. Minocycline exerts multiple inhibitory effects on vascular endothelial growth factor-induced smooth muscle cell migration: the role of ERK1/2, PI3K, and matrix metalloproteinases. Circ Res 2004, 95:364-371.
73. Yuskaitis C.J., Mines M.A., King M.K., Sweatt J.D., Miller C.A., Jope R.S. Lithium ameliorates altered glycogen synthase kinase-3 and behavior in a mouse model of Fragile X syndrome. Biochem Pharmacol 2010, 79:632-646.
74. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089.
75. Zalfa F., Achsel T., Bagni C. MRNPs, polysomes or granules: FMRP in neuronal protein synthesis. Curr Opin Neurobiol 2006, 16:265-269.