Huntingtin protein interactions altered by polyglutamine expansion as determined by quantitative proteomic analysis

Cell Cycle

Volumn 11, Issue 10, 2012, Pages 2006-2021

  Ratovitski, Tamara ^a   Chighladze, Ekaterine ^a   Arbez, Nicolas ^a   Boronina, Tatiana ^a   Herbrich, Shelley ^b   Cole, Robert N ^a   Ross, Christopher A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Huntingtin; Huntington disease mechanism; Neurodegeneration; Protein interactions; RNA processing

Indexed keywords

APOPTOSIS INDUCING FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MITOCHONDRIAL PROTEIN; POLYGLUTAMINE; PROTEIN; PROTEIN HUNTINGTIN; RIBONUCLEASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL DEATH; CELL FUNCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYO; ENERGY YIELD; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; RNA PROCESSING;

EID: 84861402086     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20423     Document Type: Article

References (80)

1. The Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993; 72:971-83; PMID:8458085; http://dx.doi.org/10. 1016/0092-8674(93)90585-E.
2. Ross CA, Margolis RL, Rosenblatt A, Ranen NG, Becher MW, Aylward E. Huntington disease and the related disorder, dentatorubral-pallidoluysian atrophy (DRPLA). Medicine (Baltimore) 1997; 76:305-38; PMID:9352736; http://dx.doi.org/10.1097/00005792-199709000-00001.
3. Ross CA, Tabrizi SJ. Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol 2011; 10:83-98; PMID:21163446; http://dx.doi.org/10.1016/S1474-4422(10)70245-3.
4. Walker FO. Huntington's disease. Lancet 2007; 369:218-28; PMID:17240289; http://dx.doi.org/10.1016/S0140-6736(07)60111-1.
5. Li W, Serpell LC, Carter WJ, Rubinsztein DC, Huntington JA. Expression and characterization of full-length human huntingtin, an elongated HEAT repeat protein. J Biol Chem 2006; 281:15916-22; PMID:16595690; http://dx.doi.org/10. 1074/jbc.M511007200.
6. Goehler H, Lalowski M, Stelzl U, Waelter S, Stroedicke M, Worm U, et al. A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol Cell 2004; 15:853-65; PMID:15383276; http://dx.doi.org/10.1016/j.molcel.2004.09.016.
7. Nucifora FC Jr, Sasaki M, Peters MF, Huang H, Cooper JK, Yamada M, et al. Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 2001; 291:2423-8; PMID:11264541; http://dx.doi.org/10.1126/science.1056784.
8. Ross CA, Poirier MA. Opinion: What is the role of protein aggregation in neurodegeneration? Nat Rev Mol Cell Biol 2005; 6:891-8; PMID:16167052; http:// dx.doi.org/10.1038/nrm1742.
9. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ, Gohler H, et al. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 2000; 97:6763-8; PMID:10823891; http://dx.doi.org/10.1073/pnas.100110097.
10. Lim J, Crespo-Barreto J, Jafar-Nejad P, Bowman AB, Richman R, Hill DE, et al. Opposing effects of polyglutamine expansion on native protein complexes contribute to SCA1. Nature 2008; 452:713-8; PMID:18337722; http://dx.doi.org/10. 1038/nature06731.
11. Zoghbi HY, Orr HT. Pathogenic mechanisms of a polyglutamine- mediated neurodegenerative disease, spino-cerebellar ataxia type 1. J Biol Chem 2009; 284:7425-9; PMID:18957430; http://dx.doi.org/10.1074/jbc.R800041200.
12. Li XJ, Li SH, Sharp AH, Nucifora FC Jr, Schilling G, Lanahan A, et al. A huntingtin-associated protein enriched in brain with implications for pathology. Nature 1995; 378:398-402; PMID:7477378; http:// dx.doi.org/10.1038/378398a0.
13. Li XJ, Sharp AH, Li SH, Dawson TM, Snyder SH, Ross CA. Huntingtin-associated protein (HAP1): discrete neuronal localizations in the brain resemble those of neuronal nitric oxide synthase. Proc Natl Acad Sci USA 1996; 93:4839-44; PMID:8643490; http:// dx.doi.org/10.1073/pnas.93.10.4839.
14. Kalchman MA, Graham RK, Xia G, Koide HB, Hodgson JG, Graham KC, et al. Huntingtin is ubiquitinated and interacts with a specific ubiquitin-conjugating enzyme. J Biol Chem 1996; 271:19385-94; PMID:8702625; http://dx.doi.org/10.1074/ jbc.271.32.19385.
15. Kalchman MA, Koide HB, McCutcheon K, Graham RK, Nichol K, Nishiyama K, et al. HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain. Nat Genet 1997; 16:44-53; PMID:9140394; http://dx.doi.org/10.1038/ng0597-44.
16. Wanker EE, Rovira C, Scherzinger E, Hasenbank R, Wälter S, Tait D, et al. HIP-I: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum Mol Genet 1997; 6:487-95; PMID:9147654; http:// dx.doi.org/10.1093/ hmg/6.3.487.
17. Li SH, Gutekunst CA, Hersch SM, Li XJ. Interaction of huntingtin-associated protein with dynactin P150Glued. J Neurosci 1998; 18:1261-9; PMID:9454836.
18. Boutell JM, Thomas P, Neal JW, Weston VJ, Duce J, Harper PS, et al. Aberrant interactions of transcriptional repressor proteins with the Huntington's disease gene product, huntingtin. Hum Mol Genet 1999; 8:1647-55; PMID:10441327; http://dx.doi.org/10.1093/hmg/8.9.1647.
19. Li SH, Cheng AL, Zhou H, Lam S, Rao M, Li H, et al. Interaction of Huntington disease protein with transcriptional activator Sp1. Mol Cell Biol 2002; 22:1277-87; PMID:11839795; http://dx.doi.org/10.1128/MCB.22.5.1277-87. 2002.
20. Harjes P, Wanker EE. The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem Sci 2003; 28:425-33; PMID:12932731; http://dx.doi.org/10.1016/S0968-0004(03)00168-3.
21. Li SH, Li XJ. Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet 2004; 20:146-54; PMID:15036808; http://dx.doi.org/10.1016/j.tig.2004.01.008.
22. Subramaniam S, Sixt KM, Barrow R, Snyder SH. Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity. Science 2009; 324:1327-30; PMID:19498170; http://dx.doi.org/10.1126/science.1172871.
23. Savas JN, Ma B, Deinhardt K, Culver BP, Restituito S, Wu L, et al. A role for huntington disease protein in dendritic RNA granules. J Biol Chem 2010; 285:13142-53; PMID:20185826; http://dx.doi. org/10.1074/jbc.M110.114561.
24. Savas JN, Makusky A, Ottosen S, Baillat D, Then F, Krainc D, et al. Huntington's disease protein contributes to RNA-mediated gene silencing through association with Argonaute and P bodies. Proc Natl Acad Sci USA 2008; 105:10820-5; PMID:18669659; http:// dx.doi.org/10.1073/pnas.0800658105.
25. Kaltenbach LS, Romero E, Becklin RR, Chettier R, Bell R, Phansalkar A, et al. Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet 2007; 3:82; PMID:17500595; http://dx.doi.org/10.1371/journal.pgen. 0030082.
26. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, Tartaglia GG, et al. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 2011; 144:67-78; PMID:21215370; http://dx.doi.org/10.1016/j.cell.2010.11.050.
27. Raychaudhuri S, Dey S, Bhattacharyya NP, Mukhopadhyay D. The role of intrinsically unstructured proteins in neurodegenerative diseases. PLoS One 2009; 4:5566; PMID:19440375; http://dx.doi.org/10.1371/journal.pone.0005566.
28. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, Lu G, et al. Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 2006; 125:1179-91; PMID:16777606; http://dx.doi.org/10. 1016/j.cell.2006.04.026.
29. Ratovitski T, Gucek M, Jiang H, Chighladze E, Waldron E, D'Ambola J, et al. Mutant huntingtin N-terminal fragments of specific size mediate aggregation and toxicity in neuronal cells. J Biol Chem 2009; 284:10855-67; PMID:19204007; http://dx.doi. org/10.1074/jbc.M804813200.
30. Ratovitski T, Nakamura M, D'Ambola J, Chighladze E, Liang Y, Wang W, et al. N-terminal proteolysis of full-length mutant huntingtin in an inducible PC12 cell model of Huntington's disease. Cell Cycle 2007; 6:2970-81; PMID:18156806; http://dx.doi. org/10.4161/cc.6.23.4992.
31. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004; 3:1154-69; PMID:15385600; http://dx.doi. org/10.1074/mcp.M400129-MCP200.
32. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, Persichetti F, et al. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 2000; 9:2799-809; PMID:11092756; http://dx.doi.org/10.1093/hmg/9.19.2799.
33. Raychaudhuri S, Sinha M, Mukhopadhyay D, Bhattacharyya NP. HYPK, a Huntingtin interacting protein, reduces aggregates and apoptosis induced by N-terminal Huntingtin with 40 glutamines in Neuro2a cells and exhibits chaperone-like activity. Hum Mol Genet 2008; 17:240-55; PMID:17947297; http:// dx.doi.org/10.1093/hmg/ddm301.
34. Hill EG, Schwacke JH, Comte-Walters S, Slate EH, Oberg AL, Eckel-Passow JE, et al. A statistical model for iTRAQ data analysis. J Proteome Res 2008; 7:3091-101; PMID:18578521; http://dx.doi.org/10.1021/pr070520u.
35. Oberg AL, Mahoney DW, Eckel-Passow JE, Malone CJ, Wolfinger RD, Hill EG, et al. Statistical analysis of relative labeled mass spectrometry data from complex samples using ANOVA. J Proteome Res 2008; 7:225-33; PMID:18173221; http://dx.doi.org/10.1021/pr700734f.
36. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003; 100:9440-5; PMID:12883005; http://dx.doi.org/10. 1073/pnas.1530509100.
37. Norberg E, Orrenius S, Zhivotovsky B. Mitochondrial regulation of cell death: processing of apoptosis-inducing factor (AIF). Biochem Biophys Res Commun 2010; 396:95-100; PMID:20494118; http://dx.doi.org/10.1016/j.bbrc.2010.02.163.
38. Shiina N, Shinkura K, Tokunaga M. A novel RNA-binding protein in neuronal RNA granules: regulatory machinery for local translation. J Neurosci 2005; 25:4420-34; PMID:15858068; http://dx.doi.org/10.1523/JNEUROSCI.0382-05.2005.
39. Solomon S, Xu Y, Wang B, David MD, Schubert P, Kennedy D, et al. Distinct structural features of caprin-1 mediate its interaction with G3BP-1 and its induction of phosphorylation of eukaryotic translation initiation factor 2alpha, entry to cytoplasmic stress granules, and selective interaction with a subset of mRNAs. Mol Cell Biol 2007; 27:2324-42; PMID:17210633; http://dx.doi.org/10. 1128/MCB.02300-06.
40. Jayaraman M, Kodali R, Sahoo B, Thakur AK, Mayasundari A, Mishra R, et al. Slow amyloid nucleation via α-helix-rich oligomeric intermediates in short polyglutamine-containing huntingtin fragments. J Mol Biol 2012; 415:881-99; PMID:22178474; http:// dx.doi.org/10.1016/j.jmb.2011.12.010.
41. Mishra R, Jayaraman M, Roland BP, Landrum E, Fullam T, Kodali R, et al. Inhibiting the nucleation of amyloid structure in a huntingtin fragment by targeting α-helix-rich oligomeric intermediates. J Mol Biol 2012; 415:900-17; PMID:22178478; http://dx.doi.org/10.1016/j.jmb.2011.12.011.
42. Kelley NW, Huang X, Tam S, Spiess C, Frydman J, Pande VS. The predicted structure of the headpiece of the Huntingtin protein and its implications on Huntingtin aggregation. J Mol Biol 2009; 388:919-27; PMID:19361448; http://dx.doi.org/10.1016/j.jmb.2009.01.032.
43. Ross CA, Poirier MA, Wanker EE, Amzel M. Polyglutamine fibrillogenesis: the pathway unfolds. Proc Natl Acad Sci USA 2003; 100:1-3; PMID:12509507; http://dx.doi.org/10.1073/pnas.0237018100.
44. Davranche A, Aviolat H, Zeder-Lutz G, Busso D, Altschuh D, Trottier Y, et al. Huntingtin affinity for partners is not changed by polyglutamine length: aggregation itself triggers aberrant interactions. Hum Mol Genet 2011; 20:2795-806; PMID:21518730; http:// dx.doi.org/10.1093/hmg/ddr178.
45. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006; 443:787-95; PMID:17051205; http://dx.doi. org/10.1038/nature05292.
46. Orr AL, Li S, Wang CE, Li H, Wang J, Rong J, et al. N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J Neurosci 2008; 28:2783-92; PMID:18337408; http:// dx.doi.org/10.1523/JNEUROSCI. 0106-08.2008.
47. Shirendeb U, Reddy AP, Manczak M, Calkins MJ, Mao P, Tagle DA, et al. Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington's disease: implications for selective neuronal damage. Hum Mol Genet 2011; 20:1438- 55; PMID:21257639; http://dx.doi.org/10.1093/hmg/ ddr024.
48. Miramar MD, Costantini P, Ravagnan L, Saraiva LM, Haouzi D, Brothers G, et al. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J Biol Chem 2001; 276:16391-8; PMID:11278689; http://dx.doi.org/10.1074/jbc.M010498200.
49. Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN, et al. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002; 419:367-74; PMID:12353028; http://dx.doi.org/10.1038/nature01034.
50. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007; 131:476-91; PMID:17981116; http://dx.doi.org/10.1016/j.cell.2007.08.047.
51. Vahsen N, Candé C, Brière JJ, Bénit P, Joza N, Larochette N, et al. AIF deficiency compromises oxidative phosphorylation. EMBO J 2004; 23:4679-89; PMID:15526035; http://dx.doi.org/10.1038/sj.emboj.7600461.
52. Candé C, Vahsen N, Kouranti I, Schmitt E, Daugas E, Spahr C, et al. AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis. Oncogene 2004; 23:1514-21; PMID:14716299; http://dx.doi.org/10.1038/sj.onc. 1207279.
53. Otera H, Ohsakaya S, Nagaura Z, Ishihara N, Mihara K. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J 2005; 24:1375-86; PMID:15775970; http://dx.doi.org/10.1038/sj.emboj.7600614.
54. Vahsen N, Candé C, Dupaigne P, Giordanetto F, Kroemer RT, Herker E, et al. Physical interaction of apoptosis-inducing factor with DNA and RNA. Oncogene 2006; 25:1763-74; PMID:16278674; http://dx.doi.org/10.1038/sj.onc. 1209206.
55. Hangen E, De Zio D, Bordi M, Zhu C, Dessen P, Caffin F, et al. A brain-specific isoform of mitochondrial apoptosis-inducing factor: AIF2. Cell Death Differ 2010; 17:1155-66; PMID:20111043; http:// dx.doi.org/10.1038/cdd. 2009.211.
56. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002; 2:647-56; PMID:12209154; http://dx.doi.org/10.1038/nrc883.
57. + ATPase subunit isoforms and leads to the degeneration of neuronal networks. J Neurosci 2010; 30:12816-30; PMID:20861386; http://dx.doi.org/10.1523/JNEUROSCI.6386-09.2010.
58. Angenstein F, Evans AM, Ling SC, Settlage RE, Ficarro S, Carrero-Martinez FA, et al. Proteomic characterization of messenger ribonucleoprotein complexes bound to nontranslated or translated poly(A) mRNAs in the rat cerebral cortex. J Biol Chem 2005; 280:6496-503; PMID:15596439; http://dx.doi.org/10.1074/jbc. M412742200.
59. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol 2007; 431:61-81; PMID:17923231; http://dx.doi.org/10.1016/S0076- 6879(07)31005-7.
60. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, et al. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 2003; 160:823-31; PMID:12642610; http://dx.doi.org/10. 1083/jcb.200212128.
61. Tourrière H, Gallouzi IE, Chebli K, Capony JP, Mouaikel J, van der Geer P, et al. RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol 2001; 21:7747-60; PMID:11604510; http:// dx.doi.org/10.1128/MCB.21.22.7747-60.2001.
62. Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol 2009; 5:311-22; PMID:19498435; http://dx.doi.org/10.1038/nrneurol.2009.54.
63. Gauthier LR, Charrin BC, Borrell-Pagès M, Dompierre JP, Rangone H, Cordelières FP, et al. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 2004; 118:127-38; PMID:15242649; http://dx.doi.org/10.1016/j.cell.2004.06. 018.
64. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, et al. Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 2001; 293:493-8; PMID:11408619; http:// dx.doi.org/10.1126/science. 1059581.
65. Ma B, Culver BP, Baj G, Tongiorgi E, Chao MV, Tanese N. Localization of BDNF mRNA with the Huntington's disease protein in rat brain. Mol Neurodegener 2010; 5:22; PMID:20507609; http:// dx.doi.org/10.1186/1750-1326-5-22.
66. Lemmens R, Moore MJ, Al-Chalabi A, Brown RH Jr, Robberecht W. RNA metabolism and the pathogenesis of motor neuron diseases. Trends Neurosci 2010; 33:249-58; PMID:20227117; http://dx.doi.org/10.1016/j.tins.2010.02.003.
67. Todd PK, Paulson HL. RNA-mediated neurodegeneration in repeat expansion disorders. Ann Neurol 2010; 67:291-300; PMID:20373340.
68. La Spada AR, Taylor JP. Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat Rev Genet 2010; 11:247-58; PMID:20177426; http:// dx.doi.org/10.1038/nrg2748.
69. Bilen J, Liu N, Bonini NM. A new role for microRNA pathways: modulation of degeneration induced by pathogenic human disease proteins. Cell Cycle 2006; 5:2835-8; PMID:17172864; http://dx.doi.org/10.4161/cc.5.24.3579.
70. Junn E, Mouradian MM. MicroRNAs in neurodegenerative disorders. Cell Cycle 2010; 9:1717-21; PMID:20404550; http://dx.doi.org/10.4161/cc.9.9.11296.
71. Lagier-Tourenne C, Polymenidou M, Cleveland DW. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 2010; 19:46-64; PMID:20400460; http://dx.doi.org/10.1093/hmg/ddq137.
72. Doumanis J, Wada K, Kino Y, Moore AW, Nukina N. RNAi screening in Drosophila cells identifies new modifiers of mutant huntingtin aggregation. PLoS One 2009; 4:7275; PMID:19789644; http://dx.doi.org/10.1371/journal.pone. 0007275.
73. Runne H, Régulier E, Kuhn A, Zala D, Gokce O, Perrin V, et al. Dysregulation of gene expression in primary neuron models of Huntington's disease shows that polyglutamine-related effects on the striatal transcriptome may not be dependent on brain circuitry. J Neurosci 2008; 28:9723-31; PMID:18815258; http:// dx.doi.org/10.1523/JNEUROSCI.3044-08.2008.
74. Sipione S, Rigamonti D, Valenza M, Zuccato C, Conti L, Pritchard J, et al. Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses. Hum Mol Genet 2002; 11:1953-65; PMID:12165557; http://dx.doi.org/10.1093/hmg/11.17.1953.
75. Tauber E, Miller-Fleming L, Mason RP, Kwan W, Clapp J, Butler NJ, et al. Functional gene expression profiling in yeast implicates translational dysfunction in mutant huntingtin toxicity. J Biol Chem 2011; 286:410-9; PMID:21044956; http://dx.doi.org/10.1074/jbc.M110.101527.
76. Wyttenbach A, Swartz J, Kita H, Thykjaer T, Carmichael J, Bradley J, et al. Polyglutamine expansions cause decreased CRE-mediated transcription and early gene expression changes prior to cell death in an inducible cell model of Huntington's disease. Hum Mol Genet 2001; 10:1829-45; PMID:11532992; http:// dx.doi.org/10.1093/hmg/10.17.1829.
77. Sharp AH, Loev SJ, Schilling G, Li SH, Li XJ, Bao J, et al. Widespread expression of Huntington's disease gene (IT15) protein product. Neuron 1995; 14:1065- 74; PMID:7748554; http://dx.doi.org/10.1016/0896-6273(95)90345-3.
78. Peters MF, Ross CA. Isolation of a 40-kDa Huntingtin-associated protein. J Biol Chem 2001; 276:3188-94; PMID:11035034; http://dx.doi.org/10.1074/jbc. M008099200.
79. Ko J, Ou S, Patterson PH. New anti-huntingtin monoclonal antibodies: implications for huntingtin conformation and its binding proteins. Brain Res Bull 2001; 56:319-29; PMID:11719267; http://dx.doi.org/10.1016/S0361-9230(01) 00599-8.
80. Schnaitman C, Greenawalt JW. Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J Cell Biol 1968; 38:158-75; PMID:5691970; http://dx.doi.org/10.1083/jcb.38.1.158.