Mutant huntingtin and glycogen synthase kinase 3-β accumulate in neuronal lipid rafts of a presymptomatic knock-in mouse model of Huntington's disease

Journal of Neuroscience Research

Volumn 88, Issue 1, 2010, Pages 179-190

  Valencia, Antonio ^a   Reeves, Patrick B ^a   Sapp, Ellen ^a   Li, Xueyi ^a   Alexander, Jonathan ^a   Kegel, Kimberly B ^a   Chase, Kathryn ^b   Aronin, Neil ^b   DiFiglia, Marian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Detergent resistant membranes; GSK3 ; Huntington; Lipid rafts; Neurodegeneration

Indexed keywords

CHOLESTEROL; DETERGENT; FLOTILLIN 1; GLYCOGEN SYNTHASE KINASE 3BETA; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HUNTINGTIN; MARKER; MUTANT PROTEIN; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASSOCIATION; BRAIN NERVE CELL; CHEMICAL ANALYSIS; CONTROLLED STUDY; HUNTINGTON CHOREA; LIPID RAFT; MEMBRANE; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL FRACTIONATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; GLYCOGEN SYNTHASE KINASE 3; HUNTINGTON DISEASE; INDOLES; MALEIMIDES; MEMBRANE MICRODOMAINS; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS;

EID: 73949155373     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22184     Document Type: Article

References (71)

1. Arcaro A, Aubert M, Espinosa del Hierro ME, Khanzada UK, Angelidou S, Tetley TD, Bittermann AG, Frame MC, Seckl MJ. 2007. Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal 19:1081-1092.
2. Aronin N, Kim M, Laforet G, DiFiglia M. 1999. Are there multiple pathways in the pathogenesis of Huntington's disease? Philos Trans R Soc Lond B Biol Sci 354:995-1003.
3. Bari M, Battista N, Fezza F, Finazzi-Agro A, Maccarrone M. 2005. Lipid rafts control signaling of type 1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis. J Biol Chem 280:12212-12220.
4. Bari M, Spagnuolo P, Fezza F, Oddi S, Pasquariello N, Finazzi-Agro A, Maccarrone M. 2006. Effect of lipid rafts on Cb2 receptor signaling and 2-arachidonoyl-glycerol metabolism in human immune cells. J Immunol 177:4971-4980.
5. Bauer B, Jenny M, Fresser F, Uberall F, Baier G. 2003. AKT1/PKBalpha is recruited to lipid rafts and activated downstream of PKC isotypes in CD3-induced T cell signaling. FEBS Lett 541:155-162.
6. Brackenridge CJ. 1971. The relation of type of initial symptoms and line of transmission to ages at onset and death in Huntington's disease. Clin Genet 2:287-297.
7. Carmichael J, Sugars KL, Bao YP, Rubinsztein DC. 2002. Glycogen synthase kinase-3β inhibitors prevent cellular polyglutamine toxicity caused by the Huntington's disease mutation. J Biol Chem 277:33791-33798.
8. Choo YS, Johnson GV, MacDonald M, Detloff PJ, Lesort M. 2004. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum Mol Genet 13:1407-1420.
9. Del Toro D, Alberch J, Lazaro-Dieguez F, Martin-Ibanez R, Xifro X, Egea G, Canals JM. 2009. Mutant huntingtin impairs post-Golgi trafficking to lysosomes by delocalizing optineurin/Rab8 complex from the Golgi apparatus. Mol Biol Cell (in press).
10. Delint-Ramirez I, Salcedo-Tello P, Bermudez-Rattoni F. 2008. Spatial memory formation induces recruitment of NMDA receptor and PSD-95 to synaptic lipid rafts. J Neurochem 106:1658-1668.
11. DiFiglia M, Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel JP, Carraway R, Reeves SA, et al. 1995. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14:1075-1081.
12. Eickholt BJ, Walsh FS, Doherty P. 2002. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in semaphorin 3A signaling. J Cell Biol 157:211-217.
13. Etienne-Manneville S, Hall A. 2003. Cdc42 regulates GSK-3b and adenomatous polyposis coli to control cell polarity. Nature 421:753-756.
14. Frame S, Cohen P. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359:1-16.
15. Friedrichson T, Kurzchalia TV. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394:802-805.
16. 2+ in transgenic Huntington disease rats. J Biol Chem 283:30715-30724.
17. Gines S, Ivanova E, Seong IS, Saura CA, MacDonald ME. 2003. Enhanced Akt signaling is an early prosurvival response that reflects N-methyl-D-aspartate receptor activation in Huntington's disease knock-in striatal cells. J Biol Chem 278:50514-50522.
18. Glass M, Faull RL, Dragunow M. 1993. Loss of cannabinoid receptors in the substantia nigra in Huntington's disease. Neuroscience 56:523-527.
19. Gniadecki R, Bang B. 2003. Flotillas of lipid rafts in transit amplifying cell-like keratinocytes. J Invest Dermatol 121:522-528.
20. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3β in cellular signaling. Prog Neurobiol 65:391-426.
21. Hahn-Barma V, Deweer B, Durr A, Dode C, Feingold J, Pillon B, Agid Y, Brice A, Dubois B. 1998. Are cognitive changes the first symptoms of Huntington's disease? A study of gene carriers. J Neurol Neurosurg Psychiatry 64:172-177.
22. Hickey MA, Kosmalska A, Enayati J, Cohen R, Zeitlin S, Levine MS, Chesselet MF. 2008. Extensive early motor and nonmotor behavioral deficits are followed by striatal neuronal loss in knock-in Huntington's disease mice. Neuroscience 157:280-295.
23. Hill MM, Feng J, Hemmings BA. 2002. Identification of a plasma membrane Raft-associated PKB Ser473 kinase activity that is distinct from ILK and PDK1. Curr Biol 12:1251-1255.
24. Huo H, Guo X, Hong S, Jiang M, Liu X, Liao K. 2003. Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction. J Biol Chem 278:11561-11569.
25. Hou Q, Huang Y, Amato S, Snyder SH, Huganir RL, Man HY. 2008. Regulation of AMPA receptor localization in lipid rafts. Mol Cell Neurosci 38:213-223.
26. Jacobowitz DM, Kallarakal AT. 2004. Flotillin-1 in the substantia nigra of the Parkinson brain and a predominant localization in catecholaminergic nerves in the rat brain. Neurotox Res 6:245-257.
27. 2+ entry and respiratory burst: correlations with calcium channel raft trafficking. J Immunol 178:5253-5261.
28. Kegel KB, Sapp E, Yoder J, Cuiffo B, Sobin L, Kim YJ, Qin ZH, Hayden MR, Aronin N, Scott DL, Isenberg G, Goldmann WH, DiFiglia M. 2005. Huntingtin associates with acidic phospholipids at the plasma membrane. J Biol Chem 280:36464-36473.
29. Kenworthy AK, Petranova N, Edidin M. 2000. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol Biol Cell 11:1645-1655.
30. Koh SH, Lee YB, Kim KS, Kim HJ, Kim M, Lee YJ, Kim J, Lee KW, Kim SH. 2005. Role of GSK-3β activity in motor neuronal cell death induced by G93A or A4V mutant hSOD1 gene. Eur J Neurosci 22:301-309.
31. Kumar N, Afeyan R, Sheppard S, Harms B, Lauffenburger DA. 2007. Quantitative analysis of Akt phosphorylation and activity in response to EGF and insulin treatment. Biochem Biophys Res Commun 354:14-20.
32. Lambert S, Vind-Kezunovic D, Karvinen S, Gniadecki R. 2006. Ligandin-dependent activation of the EGFR by lipid raft disruption. J Invest Dermatol 126:954-962.
33. Lee KY, Koh SH, Noh MY, Park KW, Lee YJ, Kim SH. 2007. Glycogen synthase kinase-3β activity plays very important roles in determining the fate of oxidative stress-inflicted neuronal cells. Brain Res 1129:89-99.
34. Li X, Sapp E, Valencia A, Kegel KB, Qin ZH, Alexander J, Masso N, Reeves P, Ritch JJ, Zeitlin S, Aronin N, Difiglia M. 2008. A function of huntingtin in guanine nucleotide exchange on Rab11. Neuroreport 19:1643-1647.
35. Lim D, Fedrizzi L, Tartari M, Zuccato C, Cattaneo E, Brini M, Carafoli E. 2008. Calcium homeostasis and mitochondrial dysfunction in striatal neurons of Huntington disease. J Biol Chem 283:5780-5789.
36. Lin CF, Chen CL, Chiang CW, Jan MS, Huang WC, Lin YS. 2007. GSK-3β acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis. J Cell Sci 120:2935-2943.
37. Lin CH, Tallaksen-Greene S, Chien WM, Cearley JA, Jackson WS, Crouse AB, Ren S, Li XJ, Albin RL, Detloff PJ. 2001. Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum Mol Genet 10:137-144.
38. Maccarrone M, De Chiara V, Gasperi V, Viscomi MT, Rossi S, Oddi S, Molinari M, Musella A, Finazzi-Agro A, Centonze D. 2009. Lipid rafts regulate 2-arachidonoylglycerol metabolism and physiological activity in the striatum. J Neurochem (in press).
39. Menalled LB, Sison JD, Dragatsis I, Zeitlin S, Chesselet MF. 2003. Time course of early motor and neuropathological anomalies in a knock-in mouse model of Huntington's disease with 140 CAG repeats. J Comp Neurol 465:11-26.
40. Milakovic T, Quintanilla RA, Johnson GV. 2006. Mutant huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. J Biol Chem 281:34785-34795.
41. Min YK, Lee JE, Chung KC. 2007. Zinc induces cell death in immortalized embryonic hippocampal cells via activation of Akt-GSK-3β signaling. Exp Cell Res 313:312-321.
42. Molander-Melin M, Blennow K, Bogdanovic N, Dellheden B, Mansson JE, Fredman P. 2005. Structural membrane alterations in Alzheimer brains found to be associated with regional disease development; increased density of gangliosides GM1 and GM2 and loss of cholesterol in detergent-resistant membrane domains. J Neurochem 92:171-182.
43. Ohyama T, Verstreken P, Ly CV, Rosenmund T, Rajan A, Tien AC, Haueter C, Schulze KL, Bellen HJ. 2007. Huntingtin-interacting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles. J Cell Biol 179:1481-1496.
44. Orr AL, Li S, Wang CE, Li H, Wang J, Rong J, Xu X, Mastroberardino PG, Greenamyre JT, Li XJ. 2008. N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J Neurosci 28:2783-2792.
45. Pal A, Severin F, Hopfner S, Zerial M. 2008. Regulation of endosome dynamics by Rab5 and Huntingtin-HAP40 effector complex in physiological vs. pathological conditions. Methods Enzymol 438:239-257.
46. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E, Wu D, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT, Collingridge GL. 2007. LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53:703-717.
47. Pike LJ. 2005. Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim Biophys Acta 1746:260-273.
48. Pike LJ. 2008. The challenge of lipid rafts. J Lipid Res (in press).
49. Pike LJ, Miller JM. 1998. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem 273:22298-22304.
50. Pike LJ, Han X, Gross RW. 2005. Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids: a shotgun lipidomics study. J Biol Chem 280:26796-26804.
51. Ponce J, de la Ossa NP, Hurtado O, Millan M, Arenillas JF, Davalos A, Gasull T. 2008. Simvastatin reduces the association of NMDA receptors to lipid rafts: a cholesterol-mediated effect in neuroprotection. Stroke 39:1269-1275.
52. Pralle A, Keller P, Florin EL, Simons K, Horber JK. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148:997-1008.
53. Puri BK, Leavitt BR, Hayden MR, Ross CA, Rosenblatt A, Greenamyre JT, Hersch S, Vaddadi KS, Sword A, Horrobin DF, Manku M, Murck H. 2005. Ethyl-EPA in Huntington disease: a double-blind, randomized, placebo-controlled trial. Neurology 65:286-292.
54. Puri BK, Bydder GM, Manku MS, Clarke A, Waldman AD, Beckmann CF. 2008. Reduction in cerebral atrophy associated with ethyl-eicosapentaenoic acid treatment in patients with Huntington's disease. J Intern Med Res 36:896-905.
55. Remijsen Q, Vanden Berghe T, Parthoens E, Asselbergh B, Vandenabeele P, Willems J. 2008. Inhibition of spontaneous neutrophil apoptosis by parabutoporin acts independently of NADPH oxidase inhibition but by lipid raft-dependent stimulation of Akt. J Leukoc Biol (in press).
56. Samhan-Arias AK, Garcia-Bereguiain MA, Martin-Romero FJ, Gutierrez-Merino C. 2009. Clustering of plasma membrane-bound cytochrome b5 reductase within "lipid raft" microdomains of the neuronal plasma membrane. Mol Cell Neurosci 40:14-26.
57. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31-39.
58. Sipione S, Rigamonti D, Valenza M, Zuccato C, Conti L, Pritchard J, Kooperberg C, Olson JM, Cattaneo E. 2002. Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses. Hum Mol Genet 11:1953-1965.
59. Song C, Perides G, Liu YF. 2002. Expression of full-length polyglutamine-expanded Huntingtin disrupts growth factor receptor signaling in rat pheochromocytoma (PC12) cells. J Biol Chem 277:6703-6707.
60. Sui Z, Kovacs AD, Maggirwar SB. 2006. Recruitment of active glycogen synthase kinase-3 into neuronal lipid rafts. Biochem Biophys Res Commun 345:1643-1648.
61. Suopanki J, Gotz C, Lutsch G, Schiller J, Harjes P, Herrmann A, Wanker EE. 2006. Interaction of huntingtin fragments with brain membranes - clues to early dysfunction in Huntington's disease. J Neurochem 96:870-884.
62. Takadera T, Ohyashiki T. 2007. Caspase-dependent apoptosis induced by calcineurin inhibitors was prevented by glycogen synthase kinase-3 inhibitors in cultured rat cortical cells. Brain Res 1133:20-26.
63. The Huntington's Disease Collaborative Research Group. 1993. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983.
64. Tong N, Sanchez JF, Maggirwar SB, Ramirez SH, Guo H, Dewhurst S, Gelbard HA. 2001. Activation of glycogen synthase kinase 3 β (GSK-3β) by platelet activating factor mediates migration and cell death in cerebellar granule neurons. Eur J Neurosci 13:1913-1922.
65. TREND-HD Study. 2008. Randomized controlled trial of ethyl- eicosapentaenoic acid in Huntington disease: the TREND-HD study. Arch Neurol 65:1582-1589.
66. Valencia A, Rajadurai A, Carle AB, Kochevar IE. 2006. 7-Dehydrocholesterol enhances ultraviolet A-induced oxidative stress in keratinocytes: roles of NADPH oxidase, mitochondria, and lipid rafts. Free Radic Biol Med 41:1704-1718.
67. Valenza M, Rigamonti D, Goffredo D, Zuccato C, Fenu S, Jamot L, Strand A, Tarditi A, Woodman B, Racchi M, Mariotti C, Di Donato S, Corsini A, Bates G, Pruss R, Olson JM, Sipione S, Tartari M, Cattaneo E. 2005. Dysfunction of the cholesterol biosynthetic pathway in Huntington's disease. J Neurosci 25:9932-9939.
68. Varma R, Mayor S. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798-801.
69. Vilhardt F, van Deurs B. 2004. The phagocyte NADPH oxidase depends on cholesterol-enriched membrane microdomains for assembly. EMBO J 23:739-748.
70. Vind-Kezunovic D, Nielsen CH, Wojewodzka U, Gniadecki R. 2008. Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells. Biochim Biophys Acta 1778:2480-2486.
71. Yanai A, Huang K, Kang R, Singaraja RR, Arstikaitis P, Gan L, Orban PC, Mullard A, Cowan CM, Raymond LA, Drisdel RC, Green WN, Ravikumar B, Rubinsztein DC, El-Husseini A, Hayden MR. 2006. Palmitoylation of huntingtin by HIP14 is essential for its trafficking and function. Nat Neurosci 9:824-831.