Challenges of Huntington's disease and quest for therapeutic biomarkers

Proteomics - Clinical Applications

Volumn 9, Issue 1-2, 2015, Pages 147-158

  Kotrcova, Eva ^a,b   Jarkovska, Karla ^a,b   Valekova, Ivona ^a,b   Zizkova, Martina ^a,b   Motlik, Jan ^a,b   Gadher, Suresh Jivan ^c   Kovarova, Hana ^a,b  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b Research Center PIGMOD   (Czech Republic)

^c Thermo Fisher Scientific   (United States)

Author keywords

HD biomarkers; Huntingtin neurotoxicity; Huntingtin pathogenesis; Huntington's disease

Indexed keywords

BIOLOGICAL MARKER; GLUTAMIC ACID; HUNTINGTIN; PROTEOME; NERVE PROTEIN;

BODY FLUID; CELL ACTIVATION; CYTOSKELETON; DISEASE COURSE; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; EXCITOTOXICITY; EXON; GENETIC REGULATION; HUMAN; HUNTINGTIN GENE; HUNTINGTON CHOREA; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; MICROGLIA; NERVE FIBER TRANSPORT; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PLURIPOTENT STEM CELL; PROGNOSIS; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; REVIEW; RODENT; TRINUCLEOTIDE REPEAT; ANIMAL; HUNTINGTON DISEASE; METABOLISM; PROCEDURES; PROTEOMICS;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; HUNTINGTON DISEASE; NERVE TISSUE PROTEINS; PROTEOME; PROTEOMICS;

EID: 84922794294     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201400073     Document Type: Review

References (87)

1. La Spada, A. R., Paulson, H. L., Fischbeck, K. H., Trinucleotide repeat expansion in neurological disease. Ann. Neurol. 1994, 36, 814-822.
2. 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, 971-983.
3. Kremer, B., Squitieri, F., Telenius, H., Andrew, S. E. et al., Molecular analysis of late onset Huntington's disease. J. Med. Genet. 1993, 30, 991-995.
4. Lee, J.-M., Ramos, E. M., Lee, J.-H., Gillis, T. et al., CAG repeat expansion in Huntington disease determines age at onset in a fully dominant fashion. Neurology 2012, 78, 690-695.
5. Van der Burg, J. M. M., Winqvist, A., Aziz, N. A., Maat-Schieman, M. L. C. et al., Gastrointestinal dysfunction contributes to weight loss in Huntington's disease mice. Neurobiol. Dis. 2011, 44, 1-8.
6. Ramos, E. M., Latourelle, J. C., Gillis, T., Mysore, J. S. et al., Candidate glutamatergic and dopaminergic pathway gene variants do not influence Huntington's disease motor onset. Neurogenetics 2013, 14, 173-179.
7. Thompson, J. A., Cruickshank, T. M., Penailillo, L. E., Lee, J. W. et al., The effects of multidisciplinary rehabilitation in patients with early-to-middle-stage Huntington's disease: a pilot study. Eur. J. Neurol. 2013, 20, 1325-1329.
8. Hersch, S. M., Rosas, H. D., Neuroprotection for Huntington's disease: ready, set, slow. Neurother. J. Am. Soc. Exp. Neurother. 2008, 5, 226-236.
9. Rosas, H. D., Chen, Y. I., Doros, G., Salat, D. H. et al., Alterations in brain transition metals in Huntington disease: an evolving and intricate story. Arch. Neurol. 2012, 69, 887-893.
10. Tsunemi, T., Ashe, T. D., Morrison, B. E., Soriano, K. R. et al., PGC-1α rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci. Transl. Med. 2012, 4, 142ra97.
11. Bürli, R. W., Luckhurst, C. A., Aziz, O., Matthews, K. L. et al., Design, synthesis, and biological evaluation of potent and selective class IIa histone deacetylase (HDAC) inhibitors as a potential therapy for Huntington's disease. J. Med. Chem. 2013, 56, 9934-9954.
12. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B. et al., Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 1996, 87, 493-506.
13. Lin, C. H., Tallaksen-Greene, S., Chien, W. M., Cearley, J. A. et al., Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum. Mol. Genet. 2001, 10, 137-144.
14. Hodgson, J. G., Agopyan, N., Gutekunst, C. A., Leavitt, B. R. et al., A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 1999, 23, 181-192.
15. Gray, M., Shirasaki, D. I., Cepeda, C., André, V. M. et al., Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J. Neurosci. 2008, 28, 6182-6195.
16. Von Hörsten, S., Schmitt, I., Nguyen, H. P., Holzmann, C. et al., Transgenic rat model of Huntington's disease. Hum. Mol. Genet. 2003, 12, 617-624.
17. Li, X.-J., Li, S., Influence of species differences on the neuropathology of transgenic Huntington's disease animal models. J. Genet. Genomics 2012, 39, 239-245.
18. Bjarkam, C. R., Jorgensen, R. L., Jensen, K. N., Sunde, N. A., Sørensen, J.-C. H., Deep brain stimulation electrode anchoring using BioGlue((R)), a protective electrode covering, and a titanium microplate. J. Neurosci. Methods 2008, 168, 151-155.
19. Jacobsen, J. C., Bawden, C. S., Rudiger, S. R., McLaughlan, C. J. et al., An ovine transgenic Huntington's disease model. Hum. Mol. Genet. 2010, 19, 1873-1882.
20. Baxa, M., Hruska-Plochan, M., Juhas, S., Vodicka, P. et al., A transgenic minipig model of Huntington's disease. J. Huntingtons Dis. 2013, 2, 47-68.
21. HD iPSC Consortium, Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 2012, 11, 264-278.
22. An, M. C., Zhang, N., Scott, G., Montoro, D. et al., Genetic correction of Huntington's disease phenotypes in induced pluripotent stem cells. Cell Stem Cell 2012, 11, 253-263.
23. Sherman, M. Y., Goldberg, A. L., Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 2001, 29, 15-32.
24. Venkatraman, P., Wetzel, R., Tanaka, M., Nukina, N., Goldberg, A. L., Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell 2004, 14, 95-104.
25. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A. et al., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441, 885-889.
26. Rosas, H. D., Salat, D. H., Lee, S. Y., Zaleta, A. K. et al., Complexity and heterogeneity: what drives the ever-changing brain in Huntington's disease? Ann. N. Y. Acad. Sci. 2008, 1147, 196-205.
27. Cicchetti, F., Prensa, L., Wu, Y., Parent, A., Chemical anatomy of striatal interneurons in normal individuals and in patients with Huntington's disease. Brain Res. Brain Res. Rev. 2000, 34, 80-101.
28. Douaud, G., Behrens, T. E., Poupon, C., Cointepas, Y. et al., In vivo evidence for the selective subcortical degeneration in Huntington's disease. NeuroImage 2009, 46, 958-966.
29. Dunah, A. W., Jeong, H., Griffin, A., Kim, Y.-M. et al., Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease. Science 2002, 296, 2238-2243.
30. Jiang, H., Nucifora, F. C., Ross, C. A., DeFranco, D. B., Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Hum. Mol. Genet. 2003, 12, 1-12.
31. Shimohata, T., Nakajima, T., Yamada, M., Uchida, C. et al., Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat. Genet. 2000, 26, 29-36.
32. Nucifora, F. C., Sasaki, M., Peters, M. F., Huang, H. et al., Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 2001, 291, 2423-2428.
33. Hu, Y., Chopra, V., Chopra, R., Locascio, J. J. et al., Transcriptional modulator H2A histone family, member Y (H2AFY) marks Huntington disease activity in man and mouse. Proc. Natl. Acad. Sci. USA 2011, 108, 17141-17146.
34. Moumné, L., Betuing, S., Caboche, J., Multiple aspects of gene dysregulation in Huntington's disease. Front. Neurol. 2013, 4, 127.
35. Browne, S. E., Bowling, A. C., MacGarvey, U., Baik, M. J. et al., Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann. Neurol. 1997, 41, 646-653.
36. Panov, A. V., Gutekunst, C.-A., Leavitt, B. R., Hayden, M. R. et al., Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat. Neurosci. 2002, 5, 731-736.
37. Lin, J., Wu, P.-H., Tarr, P. T., Lindenberg, K. S. et al., Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 2004, 119, 121-135.
38. Weydt, P., Pineda, V. V., Torrence, A. E., Libby, R. T. et al., Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab. 2006, 4, 349-362.
39. Marinkovic, P., Reuter, M. S., Brill, M. S., Godinho, L. et al., Axonal transport deficits and degeneration can evolve independently in mouse models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 2012, 109, 4296-4301.
40. Gauthier, L. R., Charrin, B. C., Borrell-Pagès, M., Dompierre, J. P. et al., Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 2004, 118, 127-138.
41. Browne, S. E., Ferrante, R. J., Beal, M. F., Oxidative stress in Huntington's disease. Brain Pathol. Zurich Switz. 1999, 9, 147-163.
42. André, V. M., Cepeda, C., Levine, M. S., Dopamine and glutamate in Huntington's disease: a balancing act. CNS Neurosci. Ther. 2010, 16, 163-178.
43. Björkqvist, M., Wild, E. J., Thiele, J., Silvestroni, A. et al., A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington's disease. J. Exp. Med. 2008, 205, 1869-1877.
44. Nayak, A., Ansar, R., Verma, S. K., Bonifati, D. M., Kishore, U., Huntington's disease: an immune perspective. Neurol. Res. Int. 2011, 2011, 563784.
45. Sapp, E., Kegel, K. B., Aronin, N., Hashikawa, T. et al., Early and progressive accumulation of reactive microglia in the Huntington disease brain. J. Neuropathol. Exp. Neurol. 2001, 60, 161-172.
46. Tai, Y. F., Pavese, N., Gerhard, A., Tabrizi, S. J. et al., Microglial activation in presymptomatic Huntington's disease gene carriers. Brain J. Neurol. 2007, 130, 1759-1766.
47. Pavese, N., Gerhard, A., Tai, Y. F., Ho, A. K. et al., Microglial activation correlates with severity in Huntington disease: a clinical and PET study. Neurology 2006, 66, 1638-1643.
48. Ellrichmann, G., Reick, C., Saft, C., Linker, R. A., The role of the immune system in Huntington's disease. Clin. Dev. Immunol. 2013, 2013, 1-11.
49. Singhrao, S. K., Neal, J. W., Morgan, B. P., Gasque, P., Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp. Neurol. 1999, 159, 362-376.
50. Rus, H., Cudrici, C., David, S., Niculescu, F., The complement system in central nervous system diseases. Autoimmunity 2006, 39, 395-402.
51. Trottier, Y., Devys, D., Imbert, G., Saudou, F. et al., Cellular localization of the Huntington's disease protein and discrimination of the normal and mutated form. Nat. Genet. 1995, 10, 104-110.
52. Cattaneo, E., Zuccato, C., Tartari, M., Normal huntingtin function: an alternative approach to Huntington's disease. Nat. Rev. Neurosci. 2005, 6, 919-930.
53. Leavitt, B. R., van Raamsdonk, J. M., Shehadeh, J., Fernandes, H. et al., Wild-type huntingtin protects neurons from excitotoxicity. J. Neurochem. 2006, 96, 1121-1129.
54. Valencia, A., Sapp, E., Kimm, J. S., McClory, H. et al., Striatal synaptosomes from Hdh(140Q/140Q) knock-in mice have altered protein levels, novel sites of methionine oxidation, and excess glutamate release after stimulation. J. Huntingtings Dis. 2013, 2, 459-475.
55. Cattaneo, E., Rigamonti, D., Goffredo, D., Zuccato, C. et al., Loss of normal huntingtin function: new developments in Huntington's disease research. Trends Neurosci. 2001, 24, 182-188.
56. Ross, C. A., Shoulson, I., Huntington disease: pathogenesis, biomarkers, and approaches to experimental therapeutics. Parkinsonism Relat. Disord. 2009, 15(Suppl 3), S135-S138.
57. Huntington Study Group, Unified Huntington's Disease Rating Scale: reliability and consistency. Mov. Disord. 1996, 11, 136-142.
58. Andre, R., Scahill, R. I., Haider, S., Tabrizi, S. J., Biomarker development for Huntington's disease. Drug Discov. Today 2014, 19, 972-979.
59. Tabrizi, S. J., Scahill, R. I., Owen, G., Durr, A. et al., Predictors of phenotypic progression and disease onset in premanifest and early-stage Huntington's disease in the TRACK-HD study: analysis of 36-month observational data. Lancet Neurol. 2013, 12, 637-649.
60. Weir, D. W., Sturrock, A., Leavitt, B. R., Development of biomarkers for Huntington's disease. Lancet Neurol. 2011, 10, 573-590.
61. Hersch, S. M., Rosas, H. D., Biomarkers to enable the development of neuroprotective therapies for huntington's disease, in: Lo, D. C., Hughes, R. E. (Eds.), Biomarkers to Enable the Development of Neuroprotective Therapies for Huntington's Disease Neurobiology of Huntington's Disease: Applications to Drug Discovery, CRC Press, Boca Raton, FL 2011.
62. Teixeira, A. L., Barbosa, I. G., Diniz, B. S., Kummer, A., Circulating levels of brain-derived neurotrophic factor: correlation with mood, cognition and motor function. Biomark. Med. 2010, 4, 871-887.
63. Zuccato, C., Marullo, M., Vitali, B., Tarditi, A. et al., Brain-derived neurotrophic factor in patients with Huntington's disease. PloS One 2011, 6, e22966.
64. Borowsky, B., Warner, J., Leavitt, B. R., Tabrizi, S. J. et al., 8OHdG is not a biomarker for Huntington disease state or progression. Neurology 2013, 80, 1934-1941.
65. Leoni, V., Long, J. D., Mills, J. A., Di Donato, S. et al., Plasma 24S-hydroxycholesterol correlation with markers of Huntington disease progression. Neurobiol. Dis. 2013, 55, 37-43.
66. Ehrnhoefer, D. E., Sutton, L., Hayden, M. R., Small changes, big impact: posttranslational modifications and function of huntingtin in Huntington disease. Neuroscientist 2011, 17, 475-492.
67. Dong, G., Callegari, E., Gloeckner, C. J., Ueffing, M., Wang, H., Mass spectrometric identification of novel posttranslational modification sites in Huntingtin. Proteomics 2012, 12, 2060-2064.
68. Tashiro, E., Zako, T., Muto, H., Itoo, Y. et al., Prefoldin protects neuronal cells from polyglutamine toxicity by preventing aggregation formation. J. Biol. Chem. 2013, 288, 19958-19972.
69. Ratovitski, T., Chighladze, E., Arbez, N., Boronina, T. et al., Huntingtin protein interactions altered by polyglutamine expansion as determined by quantitative proteomic analysis. Cell Cycle 2012, 11, 2006-2021.
70. Culver, B. P., Savas, J. N., Park, S. K., Choi, J. H. et al., Proteomic analysis of wild-type and mutant huntingtin-associated proteins in mouse brains identifies unique interactions and involvement in protein synthesis. J. Biol. Chem. 2012, 287, 21599-21614.
71. Zala, D., Hinckelmann, M.-V., Saudou, F., Huntingtin's function in axonal transport is conserved in Drosophila melanogaster. PloS One 2013, 8, e60162.
72. Shirasaki, D. I., Greiner, E. R., Al-Ramahi, I., Gray, M. et al., Network organization of the huntingtin proteomic interactome in mammalian brain. Neuron 2012, 75, 41-57.
73. Massai, L., Petricca, L., Magnoni, L., Rovetini, L. et al., Development of an ELISA assay for the quantification of soluble huntingtin in human blood cells. BMC Biochem. 2013, 14, 34.
74. Weiss, A., Abramowski, D., Bibel, M., Bodner, R. et al., Single-step detection of mutant huntingtin in animal and human tissues: a bioassay for Huntington's disease. Anal. Biochem. 2009, 395, 8-15.
75. Moscovitch-Lopatin, M., Goodman, R. E., Eberly, S., Ritch, J. J. et al., HTRF analysis of soluble huntingtin in PHAROS PBMCs. Neurology 2013, 81, 1134-1140.
76. Macdonald, D., Tessari, M. A., Boogaard, I., Smith, M. et al., Quantification assays for total and polyglutamine-expanded huntingtin proteins. PloS One 2014, 9, e96854.
77. Sorolla, M. A., Reverter-Branchat, G., Tamarit, J., Ferrer, I. et al., Proteomic and oxidative stress analysis in human brain samples of Huntington disease. Free Radic. Biol. Med. 2008, 45, 667-678.
78. Zabel, C., Mao, L., Woodman, B., Rohe, M. et al., A large number of protein expression changes occur early in life and precede phenotype onset in a mouse model for huntington disease. Mol. Cell. Proteomics 2009, 8, 720-734.
79. Zhang, J., Keene, C. D., Pan, C., Montine, K. S., Montine, T. J., Proteomics of human neurodegenerative diseases. J. Neuropathol. Exp. Neurol. 2008, 67, 923-932.
80. Saunders, N. R., Habgood, M. D., Dziegielewska, K. M., Barrier mechanisms in the brain, I. Adult brain. Clin. Exp. Pharmacol. Physiol. 1999, 26, 11-19.
81. Pan, S., Zhu, D., Quinn, J. F., Peskind, E. R. et al., A combined dataset of human cerebrospinal fluid proteins identified by multi-dimensional chromatography and tandem mass spectrometry. Proteomics 2007, 7, 469-473.
82. Enciu, A.-M., Gherghiceanu, M., Popescu, B. O., Triggers and effectors of oxidative stress at blood-brain barrier level: relevance for brain ageing and neurodegeneration. Oxid. Med. Cell. Longev. 2013, 2013, 297512.
83. Wild, E., Magnusson, A., Lahiri, N., Krus, U. et al., Abnormal peripheral chemokine profile in Huntington's disease. PLoS Curr. 2011, 3, RRN1231.
84. Silajdzic, E., Rezeli, M., Vegvari, A., Lahiri, N. et al., A critical evaluation of inflammatory markers in Huntington's disease plasma. J. Huntingtings Dis. 2013, 125-134.
85. Fang, Q., Strand, A., Law, W., Faca, V. M. et al., Brain-specific proteins decline in the cerebrospinal fluid of humans with Huntington disease. Mol. Cell. Proteomics 2008, 8, 451-466.
86. Huang, Y.-C., Wu, Y.-R., Tseng, M.-Y., Chen, Y.-C. et al., Increased prothrombin, apolipoprotein A-IV, and haptoglobin in the cerebrospinal fluid of patients with Huntington's disease. PloS One 2011, 6, e15809.
87. Kwan, W., Träger, U., Davalos, D., Chou, A. et al., Mutant huntingtin impairs immune cell migration in Huntington disease. J. Clin. Invest. 2012, 122, 4737-4747.