Progressive cognitive deficit, motor impairment and striatal pathology in a transgenic huntington disease monkey model from infancy to adulthood

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Chan, Anthony W S ^a,b   Jiang, Jie ^a,b   Chen, Yiju ^a,b   Li, Chunxia ^b   Prucha, Melinda S ^a,b   Hu, Yijuan ^c   Chi, Tim ^b   Moran, Sean ^b   Rahim, Tayeb ^b   Li, Shihua ^a   Li, Xiaojiang ^a   Zola, Stuart M ^a   Testa, Claudia M ^d   Mao, Hui ^a   Villalba, Rosa ^b   Smith, Yoland ^a,b   Zhang, Xiaodong ^b   Bachevalier, Jocelyne ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; N ACETYLASPARTIC ACID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SIZE; CELL LOSS; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; HUNTINGTON CHOREA; INFANT; LONGITUDINAL STUDY; MALE; MOTOR DYSFUNCTION; NERVE DEGENERATION; NEUROIMAGING; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PUTAMEN; RHESUS MONKEY; TRANSGENE; ANIMAL; COGNITION; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOTOR PERFORMANCE; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALIA;

ANIMALS; COGNITION; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; HUNTINGTON DISEASE; MACACA MULATTA; MALE; MOTOR SKILLS; TRANSGENES;

EID: 84930613349     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122335     Document Type: Article

References (46)

1. Brouillet E, Conde F, Beal MF, Hantraye P. Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol. 1999; 59: 427-468. PMID: 10515664
2. Pouladi MA, Morton AJ, Hayden MR. Choosing an animal model for the study of Huntington's disease. Nat Rev Neurosci. 2013; 14: 708-721. doi: 10.1038/nrn3570 PMID: 24052178
3. Chan AW, Xu Y, Jiang J, Rahim T, Zhao D, Kocerha J, Chi T, et al. A two years longitudinal study of a transgenic Huntington disease monkey. BMC Neurosci. 2014; 15: 36. doi: 10.1186/1471-2202-15-36 PMID: 24581271
4. Yang SH, Cheng PH, Banta H, Piotrowska-Nitsche K, Yang JJ, Cheng EC, et al. Towards a transgenic model of Huntington's disease in a non-human primate. Nature. 2008; 453: 921-924. doi: 10.1038/nature06975 PMID: 18488016
5. Kocerha J, Liu Y, Willoughby D, Chidamparam K, Benito J, Nelson K, et al. Longitudinal transcriptomic dysregulation in the peripheral blood of transgenic Huntington's disease monkeys. BMC Neurosci. 2013; 14: 88. doi: 10.1186/1471-2202-14-88 PMID: 23957861
6. Aylward EH, Liu D, Nopoulos PC, Ross CA, Pierson RK, Mills JA, et al. Striatal volume contributes to the prediction of onset of Huntington disease in incident cases. Biol Psychiatry. 2012; 71: 822-828. doi: 10.1016/j.biopsych.2011.07.030 PMID: 21907324
7. Paulsen JS, Nopoulos PC, Aylward E, Ross CA, Johnson H, Magnotta VA, et al. Striatal and white matter predictors of estimated diagnosis for Huntington disease. Brain Res Bull. 2010; 82: 201-207. doi: 10.1016/j.brainresbull.2010.04.003 PMID: 20385209
8. Tabrizi SJ, Scahill RI, Durr A, Roos RA, Leavitt BR, Jones R, et al. Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol. 2011; 10: 31-42. doi: 10.1016/S1474-4422(10)70276-3 PMID: 21130037
9. Tabrizi SJ, Scahill RI, Owen G, Durr A, Leavitt BR, Roos RA, 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. doi: 10.1016/S1474-4422(13)70088-7 PMID: 23664844
10. Putkhao K, Kocerha J, Cho IK, Yang J, Parnpai R, Chan AWS. Pathogenic cellular phenotypes are germline transmissible in a transgenic primate model of Huntington's disease. Stem Cells Dev. 2013; 22: 1198-1205. doi: 10.1089/scd.2012.0469 PMID: 23190281
11. Groen JL, de Bie RM, Foncke EM, Roos RA, Leenders KL, Tijssen MA. Late-onset Huntington disease with intermediate CAG repeats: true or false? J Neurol Neurosurg Psychiatry. 2010; 81: 228-230. doi: 10.1136/jnnp.2008.170902 PMID: 20145031
12. Rubinsztein DC, Leggo J, Coles R, Almqvist E, Biancalana V, Cassiman JJ, et al. Phenotypic characterization of individuals with 30-40 CAG repeats in the Huntington disease (HD) gene reveals HD cases with 36 repeats and apparently normal elderly individuals with 36-39 repeats. Am J Hum Genet. 1996; 59: 16-22. PMID: 8659522
13. Squitieri F, Jankovic J. Huntington's disease: how intermediate are intermediate repeat lengths? Mov Disord. 2012; 27: 1714-1717. doi: 10.1002/mds.25172 PMID: 23008174
14. Padowski JM, Weaver KE, Richards TL, Laurino MY, Samii A, Aylward EH, et al. Neurochemical correlates of caudate atrophy in Huntington's disease. Mov Disord. 2014; 29: 327-335. doi: 10.1002/mds.25801 PMID: 24442623
15. Unschuld PG, Edden RA, Carass A, Liu X, Shanahan M, Wang X, et al. Brain metabolite alterations and cognitive dysfunction in early Huntington's disease. Mov Disord. 2012; 27: 895-902. doi: 10.1002/mds.25010 PMID: 22649062
16. Mittoux V, Joseph JM, Conde F, Palfi S, Dautry C, Poyot T, et al. Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum Gene Ther. 2000; 11: 1177-1187. PMID: 10834619
17. Palfi S, Conde F, Riche D, Brouillet E, Dautry C, Mittoux V, et al. Fetal striatal allografts reverse cognitive deficits in a primate model of Huntington disease. Nat Med. 1998; 4: 963-966. PMID: 9701252
18. Palfi S, Ferrante RJ, Brouillet E, Beal MF, Dolan R, Guyot MC, et al. Chronic 3-nitropropionic acid treatment in baboons replicates the cognitive and motor deficits of Huntington's disease. J Neurosci. 1996; 16: 3019-3025. PMID: 8622131
19. Roitberg BZ, Emborg ME, Sramek JG, Palfi S, Kordower JH. Behavioral and morphological comparison of two nonhuman primate models of Huntington's disease. Neurosurgery. 2002; 50: 137-145; discussion 145-136. PMID: 11844244
20. Taylor JR, Elsworth JD, Roth RH, Sladek JR Jr., Redmond DE Jr. Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain. 1990; 113 (Pt 3): 617-637. PMID: 2364263
21. McBride JL, Pitzer MR, Boudreau RL, Dufour B, Hobbs T, Ojeda SR, et al. Preclinical safety of RNAi-mediated HTT suppression in the rhesus macaque as a potential therapy for Huntington's disease. Mol Ther. 2011; 19: 2152-2162. doi: 10.1038/mt.2011.219 PMID: 22031240
22. Bachevalier J, Landis LS, Walker LC, Brickson M, Mishkin M, Price DL, et al. Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiol Aging. 1991; 12: 99-111. PMID: 2052134
23. Darling WG, Peterson CR, Herrick JL, McNeal DW, Stilwell-Morecraft KS, Morecraft RJ. Measurement of coordination of object manipulation in non-human primates. J Neurosci Methods.2006; 154: 38-44. PMID: 16464505
24. Lacreuse A, Diehl MM, Goh MY, Hall MJ, Volk AM, Chhabra RK, et al. Sex differences in age-related motor slowing in the rhesus monkey: behavioral and neuroimaging data. Neurobiol Aging. 2005; 26: 543-551. PMID: 15653182
25. Zhang Z, Andersen A, Smith C, Grondin R, Gerhardt G, Gash D. Motor slowing and parkinsonian signs in aging rhesus monkeys mirror human aging. J Gerontol A Biol Sci Med Sci. 2000; 55: B473-480. PMID: 11034220
26. Biglan K, Shoulson I. Juvenile-onset huntington disease: a matter of perspective. Arch Neurol. 2007; 64: 783-784. PMID: 17562925
27. Cloud LJ, Rosenblatt A, Margolis RL, Ross CA, Pillai JA, Corey-Bloom J, Seizures in juvenile Huntington's disease: frequency and characterization in a multicenter cohort. Mov Disord. 2012; 27: 1797-1800. doi: 10.1002/mds.25237 PMID: 23124580
28. Geevasinga N, Richards FH, Jones KJ, Ryan MM. Juvenile Huntington disease. J Paediatr Child Health. 2006; 42: 552-554. PMID: 16925544
29. Squitieri F, Frati L, Ciarmiello A, Lastoria S, Quarrell O. Juvenile Huntington's disease: does a dosage-effect pathogenic mechanism differ from the classical adult disease? Mech Ageing Dev. 2006; 127: 208-212. PMID: 16274727
30. Paulsen JS, Smith MM, Long JD. Cognitive decline in prodromal Huntington Disease: implications for clinical trials. J Neurol Neurosurg Psychiatry. 2013; 84: 1233-1239. doi: 10.1136/jnnp-2013-305114 PMID: 23911948
31. Courtine G, Bunge MB, Fawcett JW, Grossman RG, Kaas JH, Lemon R, et al. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat Med. 2007; 13: 561-566. PMID: 17479102
32. Bachevalier J, Machado CJ, Kazama A. Behavioral outcomes of late-onset or early-onset orbital frontal cortex (areas 11/13) lesions in rhesus monkeys. Ann N Y Acad Sci. 2011; 1239: 71-86. doi: 10.1111/j.1749-6632.2011.06211.x PMID: 22145877
33. Ewing-Cobbs L, Prasad MR, Swank P, Kramer L, Mendez D, Treble A, et al. Social communication in young children with traumatic brain injury: Relations with corpus callosum morphometry. Int J Dev Neurosci. 2012; 30: 247-254. doi: 10.1016/j.ijdevneu.2011.07.004 PMID: 21807088
34. Rice J. Animal models: Not close enough. Nature. 2012; 484: S9-S9. PMID: 22509510
35. Aziz NA, Pijl H, Frolich M, Snel M, Streefland TC, Roelfsema F, et al. Systemic energy homeostasis in Huntington's disease patients. J Neurol Neurosurg Psychiatry. 2010; 81: 1233-1237. doi: 10.1136/jnnp.2009.191833 PMID: 20710011
36. Gaba AM, Zhang K, Marder K, Moskowitz CB, Werner P, Boozer CN. Energy balance in early-stage Huntington disease. Am J Clin Nutr. 2005; 81: 1335-1341. PMID: 15941884
37. Hamilton JM, Wolfson T, Peavy GM, Jacobson MW, Corey-Bloom J. Rate and correlates of weight change in Huntington's disease. J Neurol Neurosurg Psychiatry. 2004; 75: 209-212. PMID: 14742590
38. Sackett GP, Ruppenthal GC, Davis AE. Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). Am J Primatol. 2002; 56: 165-183. PMID: 11857653
39. Goursaud AP, Bachevalier J. Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex. Behav Brain Res. 2007; 176: 75-93. PMID: 17084912
40. Li CX, Patel S, Auerbach EJ, Zhang X. Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys. Neurosci Lett. 2013; 541: 58-62. doi: 10.1016/j.neulet.2013.02.007 PMID: 23428509
41. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004; 23 Suppl 1: S208-219. PMID: 15501092
42. Adluru N, Zhang H, Fox AS, Shelton SE, Ennis CM, Bartosic AM, et al. A diffusion tensor brain template for rhesus macaques. Neuroimage. 2012; 59: 306-318. doi: 10.1016/j.neuroimage.2011.07.029 PMID: 21803162
43. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993; 30: 672-679. PMID: 8139448
44. Haga KK, Khor YP, Farrall A, Wardlaw JM. A systematic review of brain metabolite changes, measured with 1H magnetic resonance spectroscopy, in healthy aging. Neurobiol Aging. 2009; 30: 353-363. PMID: 17719145
45. Herndon JG, Constantinidis I, Moss MB. Age-related brain changes in rhesus monkeys: a magnetic resonance spectroscopic study. Neuroreport. 1998; 9: 2127-2130. PMID: 9674606
46. Gundersen HJ. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc. 1986; 143: 3-45. PMID: 3761363