Lipid rafts: A signaling platform linking cholesterol metabolism to synaptic deficits in autism spectrum disorders

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAR, 2014, Pages

  Wang, Hansen ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Autism spectrum disorders; Cholesterol; FMRP; Fragile X syndrome; Lipid rafts; Rett syndrome; Statins; Synaptic plasticity

Indexed keywords

CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; METHYL CPG BINDING PROTEIN 2; SQUALENE MONOOXYGENASE;

ARTICLE; AUTISM; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; GLIA CELL; HUMAN; INTERPERSONAL COMMUNICATION; LIPID RAFT; MENTAL DISEASE; NERVE CELL PLASTICITY; SIGNAL TRANSDUCTION; SMITH LEMLI OPITZ SYNDROME; SOCIAL INTERACTION; STEREOTYPY; SYNAPTOGENESIS;

EID: 84897083203     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00104     Document Type: Article

References (61)

1. Allen, J. A., Halverson-Tamboli, R. A., and Rasenick, M. M. (2007). Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 8, 128-140. doi: 10.1038/nrn2059
2. Auerbach, B. D., Osterweil, E. K., and Bear, M. F. (2011). Mutations causing syndromic autism define an axis of synaptic pathophysiology. Nature 480, 63-68. doi: 10.1038/nature10658
3. Baker, S. A., Chen, L., Wilkins, A. D., Yu, P., Lichtarge, O., and Zoghbi, H. Y. (2013). An AT-hook domain in MeCP2 determines the clinical course of Rett syndrome andrelated disorders. Cell 152, 984-996. doi: 10.1016/j.cell.2013.01.038
4. Bear, M. F., Huber, K. M., and Warren, S. T. (2004). The mGluR theory of fragile X mental retardation. Trends Neurosci. 27, 370-377. doi: 10.1016/j.tins.2004.04.009
5. Buchovecky, C. M., Turley, S. D., Brown, H. M., Kyle, S. M., McDonald, J. G., Liu, B., et al. (2013). A suppressor screen in Mecp2 mutant mice implicates cholesterol metabolism in Rett syndrome. Nat. Genet. 45, 1013-1020. doi: 10.1038/ng.2714
6. Bukelis, I., Porter, F. D., Zimmerman, A. W., and Tierney, E. (2007). Smith-Lemli-Opitz syndrome and autism spectrum disorder. Am. J. Psychiatry 164, 1655-1661. doi: 10.1176/appi.ajp.2007.07020315
7. Delint-Ramirez, I., Fernandez, E., Bayes, A., Kicsi, E., Komiyama, N. H., and Grant, S. G. (2010). In vivo composition of NMDA receptor signaling complexes differs between membrane subdomains and is modulated by PSD-95 and PSD-93. J. Neurosci. 30, 8162-8170. doi: 10.1523/JNEUR0SCI.1792-10.2010
8. Delorme, R., Ey, E., Toro, R., Leboyer, M., Gillberg, C., and Bourgeron, T. (2013). Progress toward treatments for synaptic defects in autism. Nat. Med. 19, 685-694. doi: 10.1038/nm.3193
9. Diaz-Stransky, A., and Tierney, E. (2012). Cognitive and behavioral aspects of Smith-Lemli-Opitz syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 160C,295-300.doi: 10.1002/ajmg.c.31342
10. Dziobek, I., Gold, S. M., Wolf, O. T., and Convit, A. (2007). Hypercholesterolemia in Asperger syndrome: independence from lifestyle, obsessive-compulsive behavior, and social anxiety. Psychiatry Res. 149, 321-324. doi: 10.1016/j.psychres.2006.02.003
11. Ebert, D. H., and Greenberg, M. E. (2013). Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493, 327-337. doi: 10.1038/nature11860
12. Fielding, C. J., and Fielding, P. E. (2004). Membrane cholesterol and the regulation of signal transduction. Biochem. Soc. Trans. 32, 65-69. doi: 10.1042/BST0320065
13. Francesconi, A., Kumari, R., and Zukin, R. S. (2009). Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveo-lar/lipid raft pathway. J. Neurosci. 29, 3590-3602. doi: 10.1523/JNEUROSCI.5824-08.2009
14. Hering, H., Lin, C. C., and Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262-3271.
15. Huguet, G., Ey, E., and Bourgeron, T. (2013). The genetic landscapes of autism spectrum disorders. Annu. Rev. Genomics Hum. Genet. 14, 191-213. doi: 10.1146/annurev-genom-091212-153431
16. Karasinska, J. M., and Hayden, M. R. (2011). Cholesterol metabolism in Huntington disease. Nat. Rev. Neurol. 7, 561-572. doi: 10.1038/nrneu-rol.2011.132
17. Korade, Z., and Kenworthy, A. K. (2008). Lipid rafts, cholesterol, and the brain. Neuropharmacology 55, 1265-1273. doi: 10.1016/j.neuropharm.2008.02.019
18. Krumm, N., O'Roak, B. J., Shendure, J., and Eichler, E. E. (2014). A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci. 37, 95-105. doi: 10.1016/j.tins.2013.11.005
19. Kumari, R., Castillo, C., and Francesconi, A. (2009). Agonist-dependent signaling by group I metabotropic glutamate receptors is regulated by association with lipid domains. J. Biol. Chem. 288, 32004-32019. doi: 10.1074/jbc.M113.475863
20. Lee, R.W., andTierney, E. (2011). Hypothesis: therole of sterols in autism spectrum disorder. Autism Res. Treat. 2011:653570. doi: 10.1155/2011/653570
21. Levitan, I., Fang, Y., Rosenhouse-Dantsker, A., and Romanenko, V. (2010). Cholesterol and ion channels. Subcell. Biochem. 51, 509-549. doi: 10.1007/978-90-481-8622-8_19
22. Li, W., Cui, Y., Kushner, S. A., Brown, R. A., Jentsch, J. D., Frankland, P. W., et al. (2005). The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr. Biol. 15, 1961-1967. doi: 10.1016/j.cub.2005.09.043
23. Linetti, A., Fratangeli, A., Taverna, E., Valnegri, P., Francolini, M., Cappello, V., et al. (2010). Cholesterol reduction impairs exocytosis of synaptic vesicles. J. Cell Sci. 123, 595-605. doi: 10.1242/jcs.060681
24. Lingwood, D., and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50. doi: 10.1126/science.1174621
25. Liu, Q., Yao, W. D., and Suzuki, T. (2013). Specific interaction of postsynaptic densities with membrane rafts isolated from synaptic plasma membranes. J. Neurogenet. 27, 43-58. doi: 10.3109/01677063.2013.772175
26. Lyst, M. J., Ekiert, R., Ebert, D. H., Merusi, C., Nowak, J., Selfridge, J., et al. (2013). Rett syndrome mutations abolish the interaction of MeCP2 with the NCoR/SMRT co-repressor. Nat. Neurosci. 16, 898-902. doi: 10.1038/nn.3434
27. Mathews, E. S., Mawdsley, D. J., Walker, M., Hines, J. H., Pozzoli, M., and Appel, B. (2014). Mutation of 3-hydroxy-3-methylglutaryl CoA synthase I reveals requirements for isoprenoid and cholesterol synthesis in oligodendrocyte migration arrest, axon wrapping, and myelin gene expression. J. Neurosci. 34, 3402-3412. doi: 10.1523/JNEUROSCI.4587-13.2014
28. Mauch, D. H., Nagler, K., Schumacher, S., Goritz, C., Muller, E. C., Otto, A., et al. (2001). CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354-1357. doi: 10.1126/sci-ence.294.5545.1354
29. Murdoch, J. D., and State, M. W. (2013). Recent developments in the genetics of autism spectrum disorders. Curr. Opin. Genet. Dev. 23, 310-315. doi: 10.1016/j.gde.2013.02.003
30. Nagy, G., and Ackerman, S. L. (2013). Cholesterol metabolism and Rett syndrome pathogenesis. Nat. Genet. 45, 965-967. doi: 10.1038/ng.2738
31. Osterweil, E. K., Chuang, S. C., Chubykin, A. A., Sidorov, M., Bianchi, R., Wong, R. K., et al. (2013). Lovastatin corrects excess protein synthesis and prevents epileptogenesis in a mouse model of fragile X syndrome. Neuron 77, 243-250. doi: 10.1016/j.neuron.2012.01.034
32. Pani, A., Mandas, A., andDessi, S. (2010). Cholesterol, Alzheimer's disease, prion disorders: a menage a trois? Curr. Drug Targets 11, 1018-1031. doi: 10.2174/138945010791591386
33. Persico, A. M., and Napolioni, V. (2013). Autism genetics. Behav. Brain Res. 251, 95-112. doi: 10.1016/j.bbr.2013.06.012
34. Pfrieger, F. W. (2003). Cholesterol homeostasis and function in neurons of the central nervous system. Cell. Mol. Life Sci. 60, 1158-1171. doi: 10.1007/s00018-003-3018-7
35. Pfrieger, F. W., and Ungerer, N. (2011). Cholesterol metabolism in neurons and astrocytes. Prog. Lipid Res. 50, 357-371. doi: 10.1016/j.plipres.2011.06.002
36. Pristera, A., and Okuse, K. (2011). Building excitable membranes: lipid rafts and multiple controls on trafficking of electrogenic molecules. Neuroscientist 18, 70-81. doi: 10.1177/1073858410393977
37. Ronemus, M., Iossifov, I., Levy, D., and Wigler, M. (2014). The role of denovo mutations in the genetics of autism spectrum disorders. Nat. Rev. Genet. 15, 133-141. doi: 10.1038/nrg3585
38. Santoro, M. R., Bray, S. M., and Warren, S. T. (2012). Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 7, 219-245. doi: 10.1146/annurev-pathol-011811-132457
39. Schmunk, G., and Gargus, J. J. (2013). Channelopathy pathogenesis in autism spectrum disorders. Front. Genet. 4:222. doi: 10.3389/fgene.2013.00222
40. Sebastiao, A. M., Colino-Oliveira, M., Assaife-Lopes, N., Dias, R. B., and Ribeiro, J. A. (2012). Lipid rafts, synaptic transmission and plasticity: impact in age-related neurodegenerative diseases. Neuropharmacology 64, 97-107. doi: 10.1016/j.neuropharm.2012.06.053
41. Sheng, M., and Hoogenraad, C. C. (2007). The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 76, 823-847. doi: 10.1146/annurev.biochem.76.060805.160029
42. Sheng, M., and Kim, E. (2011). Thepostsynaptic organization of synapses. Cold Spring Harb. Perspect. Biol. 3:a005678. doi: 10.1101/cshperspect.a005678
43. Sikora, D. M., Pettit-Kekel, K., Penfield, J., Merkens, L. S., and Steiner, R. D. (2006). The near universal presence of autism spectrum disorders in children with Smith-Lemli-Opitz syndrome. Am. J. Med. Genet. A 140, 1511-1518. doi: 10.1002/ajmg.a.31294
44. Simons, K., and Ehehalt, R. (2002). Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110, 597-603. doi: 10.1172/JCI0216390
45. Simons, K., and Sampaio, J. L. (2011). Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 3:a004697. doi: 10.1101/cshper-spect.a004697
46. Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39. doi: 10.1038/35036052
47. Suzuki, T., Zhang, J., Miyazawa, S., Liu, Q., Farzan, M. R., and Yao, W. D. (2011). Association of membrane rafts and postsynaptic density: pro-teomics, biochemical, and ultrastructural analyses. J. Neurochem. 119, 64-77. doi: 10.1111/j.1471-4159.2011.07404.x
48. Tierney, E., Bukelis, I., Thompson, R. E., Ahmed, K., Aneja, A., Kratz, L., et al. (2006). Abnormalities of cholesterol metabolism in autism spectrum disorders. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141B, 666-668. doi: 10.1002/ajmg.b.30368
49. Tsui-Pierchala, B. A., Encinas, M., Milbrandt, J., and Johnson, E. M. Jr. (2002). Lipid rafts in neuronal signaling and function. Trends Neurosci. 25, 412-417. doi: 10.1016/S0166-2236(02) 02215-4
50. van der Most, P. J., Dolga, A. M., Nijholt, I. M., Luiten, P. G., and Eisel, U. L. (2009). Statins: mechanisms of neuroprotection. Prog. Neurobiol. 88, 64-75. doi: 10.1016/j.pneurobio.2009.02.002
51. Waage-Baudet, H., Dunty, W. C. Jr., Dehart, D.B., Hiller, S., and Sulik, K. K. (2005). Immunohistochemical and microarray analyses of a mouse model for the smith-lemli-opitz syndrome. Dev. Neurosci. 27, 378-396. doi: 10.1159/000088453
52. Wang, H., and Doering, L. C. (2013). Reversing autism by targeting downstream mTOR signaling. Front. Cell. Neurosci. 7:28. doi: 10.3389/fncel.2013.00028
53. Wang, H., Kim, S. S., and Zhuo, M. (2010). Roles of fragile X mental retardation protein in dopaminergic stimulation-induced synapse-associated protein synthesis and subsequent alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-4-propionate (AMPA) receptor internalization. J. Biol. Chem. 285, 21888-21901. doi: 10.1074/jbc.M110.116293
54. Wang, H., Wu, L. J., Kim, S. S., Lee, F. J., Gong, B., Toyoda, H., et al. (2008b). FMRP acts as a key messenger for dopamine modulation in the forebrain. Neuron 59, 634-647. doi: 10.1016/j.neuron.2008.06.027
55. Wang, H., Wu, L. J., Zhang, F., and Zhuo, M. (2008a). Roles of calcium-stimulated adenylyl cyclase and calmodulin-dependent protein kinase IV in the regulation of FMRP by group I metabotropic glutamate receptors. J. Neurosci. 28, 4385-4397. doi: 10.1523/JNEUROSCI.0646-08.2008
56. Wang, H., and Zhuo, M. (2012). Group I metabotropic glutamate receptor-mediated gene transcription and implications for synaptic plasticity and diseases. Front. Pharmacol. 3:189. doi: 10.3389/fphar.2012.00189
57. Wassif, C. A., Zhu, P., Kratz, L., Krakowiak, P. A., Battaile, K. P., Weight, F. F., et al. (2001). Biochemical, phenotypic and neurophys-iological characterization of a genetic mouse model of RSH/Smith-Lemli-Opitz syndrome. Hum. Mol. Genet. 10, 555-564. doi: 10.1093/hmg/ 10.6.555
58. Won, H., Mah, W., and Kim, E. (2013). Autism spectrum disorder causes, mechanisms, and treatments: focus on neuronal synapses. Front. Mol. Neurosci. 6:19. doi: 10.3389/fnmol.2013. 00019
59. Xu, X., and Pozzo-Miller, L. (2013). A novel DNA-binding feature of MeCP2 contributes to Rett syndrome. Front. Cell. Neurosci. 7:64. doi: 10.3389/fncel.2013.00064
60. Yaqoob, P., and Shaikh, S. R. (2010). The nutritional and clinical significance of lipid rafts. Curr. Opin. Clin. Nutr. Metab. Care 13, 156-166. doi: 10.1097/MCO.0b013e328335725b
61. Zoghbi, H. Y., and Bear, M. F. (2012). Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4:a009886. doi: 10.1101/cshperspect.a009886