AAV-dominant negative tumor necrosis factor (DN-TNF) gene transfer to the striatum does not rescue medium spiny neurons in the YAC128 mouse model of Huntington's disease

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Alto, Laura Taylor ^a   Chen, Xi ^b   Ruhn, Kelly A ^a   Treviño, Isaac ^a   Tansey, Malú G ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOMINANT NEGATIVE TUMOR NECROSIS FACTOR; GREEN FLUORESCENT PROTEIN; PARVOVIRUS VECTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE MODEL; GENE TARGETING; GENE TRANSFER; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MEDIUM SPINY NEURON; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WILD TYPE; YAC128 MOUSE; ANIMAL; GENE THERAPY; GENETICS; HUNTINGTON DISEASE; METABOLISM; MICROGLIA; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; ROTAROD TEST; TREATMENT OUTCOME;

ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; MICROGLIA; MOTOR SKILLS; NERVE DEGENERATION; NEURONS; ROTAROD PERFORMANCE TEST; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901267507     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096544     Document Type: Article

References (58)

1. Ehrlich ME (2012) Huntington's disease and the striatal medium spiny neuron: cell-autonomous and non-cell-autonomous mechanisms of disease. Neurotherapeutics 9: 270-284.
2. Gao HM, Hong JS (2008) Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 29: 357-365.
3. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG (2009) Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener 4: 47.
4. Moller T (2010) Neuroinflammation in Huntington's disease. J Neural Transm 117: 1001-1008.
5. Sapp E, Kegel KB, Aronin N, Hashikawa T, Uchiyama Y, et al. (2001) Early and progressive accumulation of reactive microglia in the Huntington disease brain. J Neuropathol Exp Neurol 60: 161-172. (Pubitemid 32172419)
6. Pavese N, Gerhard A, Tai YF, Ho AK, Turkheimer F, et al. (2006) Microglial activation correlates with severity in Huntington disease: a clinical and PET study. Neurology 66: 1638-1643. (Pubitemid 43964614)
7. Tai YF, Pavese N, Gerhard A, Tabrizi SJ, Barker RA, et al. (2007) Microglial activation in presymptomatic Huntington's disease gene carriers. Brain 130: 1759-1766. (Pubitemid 47343790)
8. Politis M, Pavese N, Tai YF, Kiferle L, Mason SL, et al. (2011) Microglial activation in regions related to cognitive function predicts disease onset in Huntington's disease: a multimodal imaging study. Hum Brain Mapp 32: 258-270.
9. Silvestroni A, Faull RL, Strand AD, Moller T (2009) Distinct neuroinflammatory profile in post-mortem human Huntington's disease. Neuroreport 20: 1098-1103.
10. Bjorkqvist M, Wild EJ, Thiele J, Silvestroni A, Andre R, et al. (2008) A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington's disease. J Exp Med 205: 1869-1877.
11. Singhrao SK, Neal JW, Morgan BP, Gasque P (1999) Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp Neurol 159: 362-376. (Pubitemid 29485223)
12. Hodges A, Strand AD, Aragaki AK, Kuhn A, Sengstag T, et al. (2006) Regional and cellular gene expression changes in human Huntington's disease brain. Hum Mol Genet 15: 965-977. (Pubitemid 43338237)
13. Dalrymple A, Wild EJ, Joubert R, Sathasivam K, Bjorkqvist M, et al. (2007) Proteomic profiling of plasma in Huntington's disease reveals neuroinflammatory activation and biomarker candidates. J Proteome Res 6: 2833-2840. (Pubitemid 47122377)
14. Leblhuber F, Walli J, Jellinger K, Tilz GP, Widner B, et al. (1998) Activated immune system in patients with Huntington's disease. Clin Chem Lab Med 36: 747-750. (Pubitemid 28521525)
15. Wild E, Magnusson A, Lahiri N, Krus U, Orth M, et al. (2011) Abnormal peripheral chemokine profile in Huntington's disease. PLoS Curr 3: RRN1231.
16. Ma L, Morton AJ, Nicholson LF (2003) Microglia density decreases with age in a mouse model of Huntington's disease. Glia 43: 274-280. (Pubitemid 37047683)
17. Crocker SF, Costain WJ, Robertson HA (2006) DNA microarray analysis of striatal gene expression in symptomatic transgenic Huntington's mice (R6/2) reveals neuroinflammation and insulin associations. Brain Res 1088: 176-186. (Pubitemid 43729411)
18. McAlpine FE, Lee JK, Harms AS, Ruhn KA, Blurton-Jones M, et al. (2009) Inhibition of soluble TNF signaling in a mouse model of Alzheimer's disease prevents pre-plaque amyloid-associated neuropathology. Neurobiol Dis 34: 163-177.
19. McCoy MK, Martinez TN, Ruhn KA, Szymkowski DE, Smith CG, et al. (2006) Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci 26: 9365-9375. (Pubitemid 44396849)
20. McCoy MK, Ruhn KA, Martinez TN, McAlpine FE, Blesch A, et al. (2008) Intranigral lentiviral delivery of dominant-negative TNF attenuates neurodegeneration and behavioral deficits in hemiparkinsonian rats. Mol Ther 16: 1572-1579.
21. Ehrlich ME, Conti L, Toselli M, Taglietti L, Fiorillo E, et al. (2001) ST14A cells have properties of a medium-size spiny neuron. Exp Neurol 167: 215-226. (Pubitemid 32150880)
22. Thompson LM, Aiken CT, Kaltenbach LS, Agrawal N, Illes K, et al. (2009) IKK phosphorylates Huntingtin and targets it for degradation by the proteasome and lysosome. J Cell Biol 187: 1083-1099.
23. Wang X, Zhu S, Drozda M, Zhang W, Stavrovskaya IG, et al. (2003) Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci U S A 100: 10483-10487. (Pubitemid 37071904)
24. Lucin KM, Wyss-Coray T (2009) Immune activation in brain aging and neurodegeneration: too much or too little? Neuron 64: 110-122.
25. Kuno R, Wang J, Kawanokuchi J, Takeuchi H, Mizuno T, et al. (2005) Autocrine activation of microglia by tumor necrosis factor-alpha. J Neuroimmunol 162: 89-96.
26. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, et al. (2006) Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: role of TNF-alpha. Faseb J 20: 670-682. (Pubitemid 44933311)
27. Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, et al. (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12: 1555-1567. (Pubitemid 36857303)
28. Lawhorn C, Smith DM, Brown LL (2008) Striosome-matrix pathology and motor deficits in the YAC128 mouse model of Huntington's disease. Neurobiol Dis 32: 471-478.
29. Menalled L, El-Khodor BF, Patry M, Suarez-Farinas M, Orenstein SJ, et al. (2009) Systematic behavioral evaluation of Huntington's disease transgenic and knock-in mouse models. Neurobiol Dis 35: 319-336.
30. Tang TS, Chen X, Liu J, Bezprozvanny I (2007) Dopaminergic signaling and striatal neurodegeneration in Huntington's disease. J Neurosci 27: 7899-7910. (Pubitemid 47173323)
31. Tang TS, Guo C, Wang H, Chen X, Bezprozvanny I (2009) Neuroprotective effects of inositol 1,4,5-trisphosphate receptor C-terminal fragment in a Huntington's disease mouse model. J Neurosci 29: 1257-1266.
32. Van Raamsdonk JM, Metzler M, Slow E, Pearson J, Schwab C, et al. (2007) Phenotypic abnormalities in the YAC128 mouse model of Huntington disease are penetrant on multiple genetic backgrounds and modulated by strain. Neurobiol Dis 26: 189-200. (Pubitemid 46436497)
33. Van Raamsdonk JM, Pearson J, Slow EJ, Hossain SM, Leavitt BR, et al. (2005) Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J Neurosci 25: 4169-4180. (Pubitemid 40563393)
34. Hodgson JG, Agopyan N, Gutekunst CA, Leavitt BR, LePiane F, et al. (1999) A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 23: 181-192. (Pubitemid 29262475)
35. Schwab C, Klegeris A, McGeer PL (2010) Inflammation in transgenic mouse models of neurodegenerative disorders. Biochim Biophys Acta 1802: 889-902.
36. Zalevsky J, Secher T, Ezhevsky SA, Janot L, Steed PM, et al. (2007) Dominant-negative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J Immunol 179: 1872-1883.
37. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, et al. (2002) Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28: 158-167. (Pubitemid 35341079)
38. Tang TS, Slow E, Lupu V, Stavrovskaya IG, Sugimori M, et al. (2005) Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc Natl Acad Sci U S A 102: 2602-2607. (Pubitemid 40279423)
39. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
40. Steed PM, Tansey MG, Zalevsky J, Zhukovsky EA, Desjarlais JR, et al. (2003) Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science 301: 1895-1898. (Pubitemid 37221393)
41. Harms AS, Barnum CJ, Ruhn KA, Varghese S, Trevino I, et al. (2011) Delayed dominant-negative TNF gene therapy halts progressive loss of nigral dopaminergic neurons in a rat model of Parkinson's disease. Mol Ther 19: 46-52.
42. Kwan W, Magnusson A, Chou A, Adame A, Carson MJ, et al. (2012) Bone marrow transplantation confers modest benefits in mouse models of Huntington's disease. J Neurosci 32: 133-142.
43. Vasileva A, Jessberger R (2005) Precise hit: adeno-associated virus in gene targeting. Nat Rev Microbiol 3: 837-847. (Pubitemid 41693179)
44. Palazuelos J, Aguado T, Pazos MR, Julien B, Carrasco C, et al. (2009) Microglial CB2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity. Brain 132: 3152-3164.
45. Stack EC, Smith KM, Ryu H, Cormier K, Chen M, et al. (2006) Combination therapy using minocycline and coenzyme Q10 in R6/2 transgenic Huntington's disease mice. Biochim Biophys Acta 1762: 373-380. (Pubitemid 43172854)
46. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, et al. (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6: 797-801. (Pubitemid 30469429)
47. Kim HS, Suh YH (2009) Minocycline and neurodegenerative diseases. Behav Brain Res 196: 168-179.
48. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21: 2580-2588. (Pubitemid 32298200)
49. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, et al. (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924. (Pubitemid 43980506)
50. Rogers JT, Morganti JM, Bachstetter AD, Hudson CE, Peters MM, et al. (2011) CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J Neurosci 31: 16241-16250.
51. Kurihara T, Warr G, Loy J, Bravo R (1997) Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J Exp Med 186: 1757-1762. (Pubitemid 27506288)
52. Rampersad RR, Tarrant TK, Vallanat CT, Quintero-Matthews T, Weeks MF, et al. (2011) Enhanced Th17-cell responses render CCR2-deficient mice more susceptible for autoimmune arthritis. PLoS One 6: e25833.
53. Perry VH (2010) Contribution of systemic inflammation to chronic neurodegeneration. Acta Neuropathol 120: 277-286.
54. Franciosi S, Ryu JK, Shim Y, Hill A, Connolly C, et al. (2012) Age-dependent neurovascular abnormalities and altered microglial morphology in the YAC128 mouse model of Huntington disease. Neurobiol Dis 45: 438-449.
55. Brambilla R, Ashbaugh JJ, Magliozzi R, Dellarole A, Karmally S, et al. (2011) Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134: 2736-2754.
56. Godavarthi SK, Narender D, Mishra A, Goswami A, Rao SN, et al. (2009) Induction of chemokines, MCP-1, and KC in the mutant huntingtin expressing neuronal cells because of proteasomal dysfunction. J Neurochem 108: 787-795.
57. Kwan W, Trager U, Davalos D, Chou A, Bouchard J, et al. (2012) Mutant huntingtin impairs immune cell migration in Huntington disease. J Clin Invest 122: 4737-4747.
58. Chou SY, Weng JY, Lai HL, Liao F, Sun SH, et al. (2008) Expanded-polyglutamine huntingtin protein suppresses the secretion and production of a chemokine (CCL5/RANTES) by astrocytes. J Neurosci 28: 3277-3290. (Pubitemid 351469331)