Partial rescue of some features of Huntington Disease in the genetic absence of caspase-6 in YAC128 mice

Neurobiology of Disease

Volumn 76, Issue , 2015, Pages 24-36

  Wong, Bibiana K Y ^a,b   Ehrnhoefer, Dagmar E ^a   Graham, Rona K ^a,c   Martin, Dale D O ^a   Ladha, Safia ^a   Uribe, Valeria ^a   Stanek, Lisa M ^d   Franciosi, Sonia ^a   Qiu, Xiaofan ^a   Deng, Yu ^a   Kovalik, Vlad ^a   Zhang, Weining ^a   Pouladi, Mahmoud A ^a,e,f   Shihabuddin, Lamya S ^d   Hayden, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

^d SANOFI   (France)

^e AGENCY FOR SCIENCE   (Singapore)

^f Dept Medicine Endocrinol Diabet   (Singapore)

Author keywords

Autophagy; Caspase 6; Huntington Disease; P62; YAC128

Indexed keywords

BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 10; CASPASE 6; CASPASE 8; PROTEIN P62; SOMATOMEDIN C; SEROTONIN TRANSPORTER; SLC6A4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CASPASE 6 GENE; CLINICAL FEATURE; CONTROLLED STUDY; CORPUS STRIATUM; EMBRYO; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE LOSS; GENE TARGETING; GENETIC ASSOCIATION; HUNTINGTON CHOREA; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; SENSITIVITY ANALYSIS; WEIGHT GAIN; ANIMAL; BODY WEIGHT; DEPRESSION; DISEASE MODEL; ENZYMOLOGY; GENETICS; METABOLISM; MOTOR ACTIVITY; TRANSGENIC MOUSE;

ANIMALS; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CASPASE 6; CORPUS STRIATUM; DEPRESSION; DISEASE MODELS, ANIMAL; HUNTINGTON DISEASE; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84922380016     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.12.030     Document Type: Article

References (70)

1. Albin R.L., et al. Abnormalities of striatal projection neurons and N-methyl-d-aspartate receptors in presymptomatic Huntington's disease. N. Engl. J. Med. 1990, 322:1293-1298.
2. Albrecht S., et al. Activation of caspase-6 in aging and mild cognitive impairment. Am. J. Pathol. 2007, 170:1200-1209.
3. Albrecht S., et al. Caspase-6 activation in familial Alzheimer disease brains carrying amyloid precursor protein or presenilin i or presenilin II mutations. J. Neuropathol. Exp. Neurol. 2009, 68:1282-1293.
4. Atwal R.S., et al. Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity. Hum. Mol. Genet. 2007, 16:2600-2615.
5. Bartlett B.J., et al. p62, Ref(2)P and ubiquitinated proteins are conserved markers of neuronal aging, aggregate formation and progressive autophagic defects. Autophagy 2011, 7:572-583.
6. Bjorkoy G., et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 2005, 171:603-614.
7. Carroll J.B., et al. Mice lacking caspase-2 are protected from behavioral changes, but not pathology, in the YAC128 model of Huntington disease. Mol. Neurodegener. 2011, 6:59.
8. Caserta T.M., et al. Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 2003, 8:345-352.
9. Cusack C.L., et al. Distinct pathways mediate axon degeneration during apoptosis and axon-specific pruning. Nat. Commun. 2013, 4:1876.
10. Dey N.D., et al. Genetically engineered mesenchymal stem cells reduce behavioral deficits in the YAC 128 mouse model of Huntington's disease. Behav. Brain Res. 2010, 214:193-200.
11. DiFiglia M., et al. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997, 277:1990-1993.
12. Dragatsis I., et al. Inactivation of Hdh in the brain and testis results in progressive neurodegeneration and sterility in mice. Nat. Genet. 2000, 26:300-306.
13. Ehrnhoefer D.E., et al. A quantitative method for the specific assessment of caspase-6 activity in cell culture. PLoS ONE 2011, 6:e27680.
14. Ehrnhoefer D.E., et al. Convergent pathogenic pathways in Alzheimer's and Huntington's diseases: shared targets for drug development. Nat. Rev. Drug Discov. 2011, 10:853-867.
15. Ferrer I., et al. Brain-derived neurotrophic factor in Huntington disease. Brain Res. 2000, 866:257-261.
16. Gafni J., et al. Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J. Biol. Chem. 2004, 279:20211-20220.
17. Gafni J., et al. Caspase-6 activity in a BACHD mouse modulates steady-state levels of mutant huntingtin protein but is not necessary for production of a 586 amino acid proteolytic fragment. J. Neurosci. 2012, 32:7454-7465.
18. Gharami K., et al. Brain-derived neurotrophic factor over-expression in the forebrain ameliorates Huntington's disease phenotypes in mice. J. Neurochem. 2008, 105:369-379.
19. Graham R.K., et al. Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 2006, 125:1179-1191.
20. Graham R.K., et al. Levels of mutant huntingtin influence the phenotypic severity of Huntington disease in YAC128 mouse models. Neurobiol. Dis. 2006, 21:444-455.
21. Graham R.K., et al. Cleavage at the 586 amino acid caspase-6 site in mutant huntingtin influences caspase-6 activation in vivo. J. Neurosci. 2010, 30:15019-15029.
22. Graham R.K., et al. Caspase-6 and neurodegeneration. Trends Neurosci. 2011, 34:646-656.
23. Graham R.K., et al. Caspase-6-resistant mutant huntingtin does not rescue the toxic effects of caspase-cleavable mutant huntingtin in vivo. JHD 2012, 1:243-260.
24. Guo H., et al. Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am. J. Pathol. 2004, 165:523-531.
25. Harper B. Huntington disease. J. R. Soc. Med. 2005, 98:550.
26. Heng M.Y., et al. Early autophagic response in a novel knock-in model of Huntington disease. Hum. Mol. Genet. 2010, 19:3702-3720.
27. Hermel E., et al. Specific caspase interactions and amplification are involved in selective neuronal vulnerability in Huntington's disease. Cell Death Differ. 2004, 11:424-438.
28. Houde C., et al. Caspase-7 expanded function and intrinsic expression level underlies strain-specific brain phenotype of caspase-3-null mice. J. Neurosci. 2004, 24:9977-9984.
29. Kennedy N.J., et al. Caspase activation is required for T cell proliferation. J. Exp. Med. 1999, 190:1891-1896.
30. Kim Y.J., et al. Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12784-12789.
31. Klionsky D.J., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
32. Krajewska M., et al. Neuronal deletion of caspase 8 protects against brain injury in mouse models of controlled cortical impact and kainic acid-induced excitotoxicity. PLoS ONE 2011, 6:e24341.
33. Landles C., et al. Caspase-6 does not contribute to the proteolysis of mutant huntingtin in the HdhQ150 knock-in mouse model of Huntington's disease. PLoS Curr. 2012, 4. (e4fd085bfc9973).
34. MacFarlane M. Compensatory caspase activation: a cautionary tale. Trends Pharmacol. Sci. 2001, 22:60.
35. Maglione V., et al. Huntingtin fragmentation and increased caspase 3, 8 and 9 activities in lymphoblasts with heterozygous and homozygous Huntington's disease mutation. Mech. Ageing Dev. 2006, 127:213-216.
36. Martin D.D., et al. Autophagy in Huntington disease and huntingtin in autophagy. Trends Neurosci. 2015, 38:26-35.
37. Martinez-Vicente M., et al. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat. Neurosci. 2010, 13:567-576.
38. Mayhew T.M., Olsen D.R. Magnetic resonance imaging (MRI) and model-free estimates of brain volume determined using the Cavalieri principle. J. Anat. 1991, 178:133-144.
39. McStay G.P., Green D.R. Measuring apoptosis: caspase inhibitors and activity assays. Cold Spring Harb. Protoc. 2014, 2014:799-806.
40. McStay G.P., et al. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ. 2008, 15:322-331.
41. Metzler M., et al. Phosphorylation of huntingtin at Ser421 in YAC128 neurons is associated with protection of YAC128 neurons from NMDA-mediated excitotoxicity and is modulated by PP1 and PP2A. J. Neurosci. 2010, 30:14318-14329.
42. Milnerwood A.J., et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
43. Monnier P.P., et al. Involvement of caspase-6 and caspase-8 in neuronal apoptosis and the regenerative failure of injured retinal ganglion cells. J. Neurosci. 2011, 31:10494-10505.
44. Pla P., et al. Huntingtin acts non cell-autonomously on hippocampal neurogenesis and controls anxiety-related behaviors in adult mouse. PLoS ONE 2013, 8:e73902.
45. Pouladi M.A., et al. Prevention of depressive behaviour in the YAC128 mouse model of Huntington disease by mutation at residue 586 of huntingtin. Brain 2009, 132:919-932.
46. Pouladi M.A., et al. Full-length huntingtin levels modulate body weight by influencing insulin-like growth factor 1 expression. Hum. Mol. Genet. 2010, 19:1528-1538.
47. Rohn T.T., et al. Activation of caspase-8 in the Alzheimer's disease brain. Neurobiol. Dis. 2001, 8:1006-1016.
48. Rue L., et al. Brain region- and age-dependent dysregulation of p62 and NBR1 in a mouse model of Huntington's disease. Neurobiol. Dis. 2013, 52:219-228.
49. Slow E.J., et al. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 2003, 12:1555-1567.
50. Sonmez O.F., et al. A stereological study of MRI and the Cavalieri principle combined for diagnosis and monitoring of brain tumor volume. J. Clin. Neurosci. 2010, 17:1499-1502.
51. Tanida I. Autophagy basics. Microbiol. Immunol. 2011, 55:1-11.
52. 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.
53. Uribe V., et al. Rescue from excitotoxicity and axonal degeneration accompanied by age-dependent behavioral and neuroanatomical alterations in caspase-6-deficient mice. Hum. Mol. Genet. 2012, 21:1954-1967.
54. van Raam B.J., et al. Intrinsic cleavage of receptor-interacting protein kinase-1 by caspase-6. Cell Death Differ. 2013, 20:86-96.
55. Van Raamsdonk J.M., et al. Selective degeneration and nuclear localization of mutant huntingtin in the YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 2005, 14:3823-3835.
56. Van Raamsdonk J.M., et al. Loss of wild-type huntingtin influences motor dysfunction and survival in the YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 2005, 14:1379-1392.
57. Van Raamsdonk J.M., et al. Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J. Neurosci. 2005, 25:4169-4180.
58. Van Raamsdonk J.M., et al. Body weight is modulated by levels of full-length huntingtin. Hum. Mol. Genet. 2006, 15:1513-1523.
59. Van Raamsdonk J.M., et al. Phenotypic abnormalities in the YAC128 mouse model of Huntington disease are penetrant on multiple genetic backgrounds and modulated by strain. Neurobiol. Dis. 2007, 26:189-200.
60. Van Raamsdonk J.M., et al. Testicular degeneration in Huntington disease. Neurobiol. Dis. 2007, 26:512-520.
61. Vidal R.L., et al. Targeting the UPR transcription factor XBP1 protects against Huntington's disease through the regulation of FoxO1 and autophagy. Hum. Mol. Genet. 2012, 21:2245-2262.
62. Vonsattel J.P., et al. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44:559-577.
63. Waldron-Roby E., et al. Transgenic mouse model expressing the caspase 6 fragment of mutant huntingtin. J. Neurosci. 2012, 32:183-193.
64. Warby S.C., et al. Activated caspase-6 and caspase-6-cleaved fragments of huntingtin specifically colocalize in the nucleus. Hum. Mol. Genet. 2008, 17:2390-2404.
65. Wellington C.L., et al. Caspase cleavage of gene products associated with triplet expansion disorders generates truncated fragments containing the polyglutamine tract. J. Biol. Chem. 1998, 273:9158-9167.
66. Wellington C.L., et al. Inhibiting caspase cleavage of huntingtin reduces toxicity and aggregate formation in neuronal and nonneuronal cells. J. Biol. Chem. 2000, 275:19831-19838.
67. Wellington C.L., et al. Caspase cleavage of mutant huntingtin precedes neurodegeneration in Huntington's disease. J. Neurosci. 2002, 22:7862-7872.
68. Xie Y., et al. BDNF overexpression in the forebrain rescues Huntington's disease phenotypes in YAC128 mice. J. Neurosci. 2010, 30:14708-14718.
69. Zhang X., et al. Caspase-8 expression and proteolysis in human brain after severe head injury. FASEB J. 2003, 17:1367-1369.
70. Zheng T.S., et al. Deficiency in caspase-9 or caspase-3 induces compensatory caspase activation. Nat. Med. 2000, 6:1241-1247.