Striatal synaptosomes from Hdh140Q/140Q knock-in mice have altered protein levels, novel sites of methionine oxidation, and excess glutamate release after stimulation

Journal of Huntington's Disease

Volumn 2, Issue 4, 2013, Pages 459-475

  Valencia, Antonio ^a   Sapp, Ellen ^a   Kimm, Jeffrey S ^a   McClory, Hollis ^a   Ansong, Kwadwo A ^a   Yohrling, George ^b   Kwak, Seung ^c   Kegel, Kimberly B ^a   Green, Karin M ^d   Shaffer, Scott A ^d   Aronin, Neil ^d   DiFiglia, Marian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Huntington's Dis Society of America   (United States)

^c CHDI MANAGEMENT CHDI FOUNDATION   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Glutamate release; HD; Mass spectrometry; Methionine oxidation; Mutant huntingtin; Oxidative damage; Synaptic proteins; Synaptosomes

Indexed keywords

GLUTAMIC ACID; HDH PROTEIN, MOUSE; METHIONINE; NERVE PROTEIN; NUCLEAR PROTEIN;

ANIMAL; ARTICLE; C57BL MOUSE; CORPUS STRIATUM; DISEASE MODEL; GENE TARGETING; GENETICS; HUNTINGTON CHOREA; LIQUID CHROMATOGRAPHY; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; SECRETION (PROCESS); SYNAPTOSOME; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; GENE KNOCK-IN TECHNIQUES; GLUTAMIC ACID; HUNTINGTON DISEASE; METHIONINE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OXIDATION-REDUCTION; SYNAPTOSOMES; TANDEM MASS SPECTROMETRY;

EID: 84906929787     PISSN: 18796397     EISSN: 18796400     Source Type: Journal    
DOI: 10.3233/JHD-130080     Document Type: Article

References (56)

1. DiFiglia M, Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel JP, Carraway R, Reeves SA, et al. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron. 1995;14(5): 1075-81.
2. Smith R, Brundin P, Li JY. Synaptic dysfunction in Huntington’s disease: A new perspective. Cell Mol Life Sci. 2005;62(17):1901-12.
3. Rozas JL, Gomez-Sanchez L, Tomas-Zapico C, Lucas JJ, Fernandez-Chacon R. Presynaptic dysfunction in Huntington’s disease. Biochem Soc Trans. 2010;38(2):488-92.
4. Nithianantharajah J, Hannan AJ. Dysregulation of synaptic proteins, dendritic spine abnormalities and pathological plasticity of synapses as experience-dependent mediators of cognitive and psychiatric symptoms in Huntington’s disease. Neuroscience. 2013;251:66-74.
5. Block-Galarza J, Chase KO, Sapp E, Vaughn KT, Vallee RB, DiFiglia M, Aronin N. Fast transport and retrograde movement of huntingtin and HAP 1 in axons. Neuroreport. 1997;8(9-10):2247-51.
6. Xu Q, Huang S, Song M, Wang CE, Yan S, Liu X, Gaertig MA, Yu SP, Li H, Li S, Li XJ. Synaptic mutant huntingtin inhibits synapsin-1 phosphorylation and causes neurological symptoms. J Cell Biol. 2013;202(7):1123-38.
7. Kegel-Gleason KB. Huntingtin interactions with membrane phospholipids: Strategic targets for therapeutic intervention. J Huntington’s Disease. 2013;2:239-50.
8. Kegel KB, Sapp E, Alexander J, Valencia A, Reeves P, Li X, Masso N, Sobin L, Aronin N, DiFiglia M. Polyglutamine expansion in huntingtin alters its interaction with phospholipids. J Neurochem. 2009;110(5):1585-97.
9. Valencia A, Reeves PB, Sapp E, Li X, Alexander J, Kegel KB, Chase K, Aronin N, DiFiglia M. Mutant huntingtin and glycogen synthase kinase 3-beta accumulate in neuronal lipid rafts of a presymptomatic knock-in mouse model of Huntington’s disease. J Neurosci Res. 2010;88(1):179-90.
10. Kaltenbach LS, Romero E, Becklin RR, Chettier R, Bell R, Phansalkar A, Strand A, Torcassi C, Savage J, Hurlburt A, Cha GH, Ukani L, Chepanoske CL, Zhen Y, Sahasrabudhe S, Olson J, Kurschner C, Ellerby LM, Peltier JM, Botas J, Hughes RE. Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet. 2007;3(5):e82.
11. Romero E, Cha GH, Verstreken P, Ly CV, Hughes RE, Bellen HJ, Botas J. Suppression of neurodegeneration and increased neurotransmission caused by expanded full-length huntingtin accumulating in the cytoplasm. Neuron. 2008;57(1):27-40.
12. Menalled LB, Sison JD, Dragatsis I, Zeitlin S, Chesselet MF. 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. 2003;465(1):11-26.
13. Hickey MA, Kosmalska A, Enayati J, Cohen R, Zeitlin S, Levine MS, Chesselet MF. Extensive early motor and nonmotor behavioral deficits are followed by striatal neuronal loss in knock-in Huntington’s disease mice. Neuroscience. 2008;157(1):280-95.
14. Bauer B, Jenny M, Fresser F, Uberall F, Baier G. AKT1/PKBalpha is recruited to lipid rafts and activated downstream of PKC isotypes in CD3-induced T cell signaling. FEBS Lett. 2003;541(1-3):155-62.
15. Huo H, Guo X, Hong S, Jiang M, Liu X, Liao K. Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction. J Biol Chem. 2003;278(13):11561-9.
16. Pike LJ, Han X, Gross RW. 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. 2005;280(29):26796-804.
17. Hill MM, Feng J, Hemmings BA. Identification of a plasma membrane Raft-associated PKB Ser473 kinase activity that is distinct from ILK and PDK1. Curr Biol. 2002;12(14):1251-5.
18. Arcaro A, Aubert M, Espinosa del Hierro ME, Khanzada UK, Angelidou S, Tetley TD, Bittermann AG, Frame MC, Seckl MJ. Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal. 2007;19(5):1081-92.
19. Li X, Valencia A, Sapp E, Masso N, Alexander J, Reeves P, Kegel KB, Aronin N, Difiglia M. Aberrant Rab11-dependent trafficking of the neuronal glutamate transporter EAAC1 causes oxidative stress and cell death in Huntington’s disease. J Neurosci. 2010;30(13):4552-61.
20. Hajos F. An improved method for the preparation of synaptosomal fractions in high purity. Brain Res. 1975;93(3):485-9.
21. Valencia A, Sapp E, Kimm JS, McClory H, Reeves PB, Alexander J, Ansong KA, Masso N, Frosch MP, Kegel KB, Li X, Difiglia M. Elevated NADPH oxidase activity contributes to oxidative stress and cell death in Huntington’s disease. Hum Mol Genet. 2013;22(6):1112-31.
22. McClure-Begley TD, King NM, Collins AC, Stitzel JA, Wehner JM, Butt CM. Acetylcholine-stimulated [3H]GABA release from mouse brain synaptosomes is modulated by alpha4beta2 and alpha4alpha5beta2 nicotinic receptor subtypes. Mol Pharmacol. 2009;75(4):918-26.
23. HillMP, Brotchie JM. Control of glutamate release by calcium channels and kappa-opioid receptors in rodent and primate striatum. Br J Pharmacol. 1999;127(1):275-83.
24. Valencia A, Sapp E, Reeves PB, Alexander J, Masso N, Li X, Kegel KB, DiFiglia M. Reagents that block neuronal death from Huntington’s disease also curb oxidative stress. Neuroreport. 2012;23(1):10-5.
25. Olsen JV, Schwartz JC, Griep-Raming J, Nielsen ML, Damoc E, Denisov E, Lange O, Remes P, Taylor D, Splendore M, Wouters ER, Senko M, Makarov A, Mann M, Horning S. A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol Cell Proteomics. 2009; 8(12):2759-69.
26. Second TP, Blethrow JD, Schwartz JC, Merrihew GE, Mac-Coss MJ, Swaney DL, Russell JD, Coon JJ, Zabrouskov V. Dual-pressure linear ion trap mass spectrometer improving the analysis of complex protein mixtures. Anal Chem. 2009;81(18):7757-65.
27. Searle BC. Scaffold: A bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics. 2010;10(6):1265-9.
28. Radulovic D, Jelveh S, Ryu S, Hamilton TG, Foss E, Mao Y, Emili A. Informatics platform for global proteomic profiling and biomarker discovery using liquid chromatographytandem mass spectrometry. Mol Cell Proteomics. 2004; 3(10):984-97.
29. Krauss S, Griesche N, Jastrzebska E, Chen C, Rutschow D, Achmuller C, Dorn S, Boesch SM, Lalowski M, Wanker E, Schneider R, Schweiger S. Translation of HTT mRNA with expanded CAG repeats is regulated by the MID1-PP2A protein complex. Nat Commun. 2013;4:1511.
30. Smith R, Klein P, Koc-Schmitz Y, Waldvogel HJ, Faull RL, Brundin P, Plomann M, Li JY. Loss of SNAP-25 and rabphilin 3a in sensory-motor cortex in Huntington’s disease. J Neurochem. 2007;103(1):115-23.
31. Freeman W, Morton AJ. Regional and progressive changes in brain expression of complexin II in a mouse transgenic for the Huntington’s disease mutation. Brain Res Bull. 2004;63(1):45-55.
32. Goto S, Hirano A. Synaptophysin expression in the striatum in Huntington’s disease. Acta Neuropathol. 1990;80(1):88-91.
33. Cepeda C, Hurst RS, Calvert CR, Hernandez-Echeagaray E, Nguyen OK, Jocoy E, Christian LJ, Ariano MA, Levine MS. Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington’s disease. J Neurosci. 2003;23(3):961-9.
34. Nithianantharajah J, Barkus C, MurphyM, Hannan AJ. Geneenvironment interactions modulating cognitive function and molecular correlates of synaptic plasticity in Huntington’s disease transgenic mice. Neurobiol Dis. 2008;29(3): 490-504.
35. Rozas JL, Gomez-Sanchez L, Tomas-Zapico C, Lucas JJ, Fernandez-Chacon R. Increased neurotransmitter release at the neuromuscular junction in a mouse model of polyglutamine disease. J Neurosci. 2011;31(3):1106-13.
36. Jacobsson G, Piehl F, Meister B. VAMP-1 and VAMP-2 gene expression in rat spinal motoneurones: Differential regulation after neuronal injury. Eur J Neurosci. 1998;10(1):301-16.
37. Bao J, Sharp AH, Wagster MV, Becher M, Schilling G, Ross CA, Dawson VL, Dawson TM. Expansion of polyglutamine repeat in huntingtin leads to abnormal protein interactions involving calmodulin. Proc Natl Acad Sci U S A. 1996;93(10):5037-42.
38. Dai Y, Dudek NL, Li Q, Fowler SC, Muma NA. Striatal expression of a calmodulin fragment improved motor function, weight loss, and neuropathology in the R6/2 mouse model of Huntington’s disease. J Neurosci. 2009;29(37):11550-9.
39. Dudek NL, Dai Y, Muma NA. Neuroprotective effects of calmodulin peptide 76-121aa: Disruption of calmodulin binding to mutant huntingtin. Brain Pathol. 2010;20(1): 176-89.
40. Zainelli GM, Ross CA, Troncoso JC, Fitzgerald JK, Muma NA. Calmodulin regulates transglutaminase 2 cross-linking of huntingtin. J Neurosci. 2004;24(8):1954-61.
41. Pal A, Severin F, Hopfner S, Zerial M. Regulation of endosome dynamics by Rab5 and Huntingtin-HAP40 effector complex in physiological versus pathological conditions. Methods Enzymol. 2008;438:239-57.
42. Pal A, Severin F, Lommer B, Shevchenko A, Zerial M. Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington’s disease. J Cell Biol. 2006;172(4):605-18.
43. Doig NM, Moss J, Bolam JP. Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum. J Neurosci. 2010;30(44):14610-8.
44. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A. 2004;101(18):7158-63.
45. Calabresi P, De Murtas M, Pisani A, Stefani A, Sancesario G, Mercuri NB, Bernardi G. Vulnerability of medium spiny striatal neurons to glutamate: Role of Na+/K + ATPase. Eur J Neurosci. 1995;7(8):1674-83.
46. Luthi-Carter R, Apostol BL, Dunah AW, DeJohn MM, Farrell LA, Bates GP, Young AB, Standaert DG, Thompson LM, Cha JH. Complex alteration of NMDA receptors in transgenic Huntington’s disease mouse brain: Analysis of mRNA and protein expression, plasma membrane association, interacting proteins, and phosphorylation. Neurobiol Dis. 2003;14(3):624-36.
47. Nakagawa T, Engler JA, Sheng M. The dynamic turnover and functional roles of alpha-actinin in dendritic spines. Neuropharmacology. 2004;47(5):734-45.
48. Graveland GA, Williams RS, DiFiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington’s disease. Science. 1985;227(4688):770-3.
49. Rong J, McGuire JR, Fang ZH, Sheng G, Shin JY, Li SH, Li XJ. Regulation of intracellular trafficking of huntingtin-associated protein-1 is critical for TrkA protein levels and neurite outgrowth. J Neurosci. 2006;26(22):6019-30.
50. Andre VM, Cepeda C, Fisher YE, Huynh M, Bardakjian N, Singh S, YangXW, Levine MS. Differential electrophysiological changes in striatal output neurons in Huntington’s disease. J Neurosci. 2011;31(4):1170-82.
51. Andre VM, Fisher YE, Levine MS. Altered balance of activity in the striatal direct and indirect pathways in mouse models of Huntington’s disease. Front Syst Neurosci. 2011;5:46.
52. Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Di Simplicio P, Colombo R, Milzani A. Methionine oxidation as a major cause of the functional impairment of oxidized actin. Free Radic Biol Med. 2002;32(9):927-37.
53. Lim JC, Kim G, Levine RL. Stereospecific oxidation of calmodulin by methionine sulfoxide reductase A. Free Radic Biol Med. 2013;61C:257-64.
54. Hoshi T, Heinemann S. Regulation of cell function by methionine oxidation and reduction. J Physiol. 2001;531(Pt 1):1-11.
55. Hsu YR, Narhi LO, Spahr C, Langley KE, Lu HS. In vitro methionine oxidation of Escherichia coli-derived human stem cell factor: Effects on the molecular structure, biological activity, and dimerization. Protein Sci. 1996;5(6):1165-73.
56. Klein JC, Moen RJ, Smith EA, Titus MA, Thomas DD. Structural and functional impact of site-directed methionine oxidation in myosin. Biochemistry. 2011;50(47): 10318-27.