Effects of deletion of mutant huntingtin in steroidogenic factor 1 neurons on the psychiatric and metabolic phenotype in the BACHD mouse model of huntington disease

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Baldo, Barbara ^a   Cheong, Rachel Y ^a   Petersén, Åsa ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; INSULIN; LEPTIN; STEROIDOGENIC FACTOR 1; SEROTONIN TRANSPORTER; SLC6A4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BODY FAT; BODY WEIGHT; CONTROLLED STUDY; CROSS BREEDING; DEPRESSION; ELEVATED PLUS MAZE TEST; FEMALE; FORCED SWIM TEST; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; HORMONE BLOOD LEVEL; HTT GENE; HUNTINGTON CHOREA; INSULIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; NOVELTY SUPPRESSED FEEDING TEST; PATHOGENESIS; PHENOTYPE; ZONA INCERTA; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MOTOR ACTIVITY; MUTATION; NERVE CELL; TRANSGENIC MOUSE;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DEPRESSION; DISEASE MODELS, ANIMAL; FEMALE; GENE DELETION; GENE EXPRESSION; HUMANS; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; NEURONS; PHENOTYPE; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STEROIDOGENIC FACTOR 1;

EID: 84907522142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107691     Document Type: Article

References (52)

1. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
2. Ross CA, Aylward EH, Wild E.J., Langbehn DR, Long JD, et al. (2014) Huntington disease: natural history, biomarkers and prospects for therapeutics. Nat Rev Neurol 10: 204-216.
3. Sturrock A, Leavitt B.R. (2010) The clinical and genetic features of Huntington disease. J Geriatr Psychiatry Neurol 23: 243-259.
4. Petersen A, Gabery S. (2012) Hypothalamic and limbic system changes in Huntington's disease. Journal of Huntington's disease 1: 5-16.
5. de la Monte SM, Vonsattel JP, Richardson EP Jr (1988) Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. J Neuropathol Exp Neurol 47: 516-525.
6. Graveland GA, Williams RS, DiFiglia M. (1985) Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 227: 770-773.
7. Swaab DF (2004) Neuropeptides in hypothalamic neuronal disorders. Int Rev Cytol 240: 305-375.
8. Gabery S, Murphy K, Schultz K., Loy CT, McCusker E, et al. (2010) Changes in key hypothalamic neuropeptide populations in Huntington disease revealed by neuropathological analyses. Acta neuropathologica 120: 777-788.
9. Aziz A, Fronczek R, Maat-Schieman M, Unmehopa U., Roelandse F, et al. (2008) Hypocretin and melanin-concentrating hormone in patients with Huntington disease. Brain pathology 18: 474-483.
10. Timmers HJ, Swaab DF, van de Nes JA, Kremer HP (1996) Somatostatin 1-12 immunoreactivity is decreased in the hypothalamic lateral tuberal nucleus of Huntington's disease patients. Brain research 728: 141-148.
11. Petersen A, Gil J, Maat-Schieman ML, Bjorkqvist M., Tanila H, et al. (2005) Orexin loss in Huntington's disease. Human molecular genetics 14: 39-47.
12. Soneson C, Fontes M, Zhou Y., Denisov V, Paulsen JS, et al (2010) Early changes in the hypothalamic region in prodromal Huntington disease revealed by MRI analysis. Neurobiology of disease 40: 531-543.
13. Politis M, Pavese N, Tai Y.F., Tabrizi SJ, Barker RA, et al. (2008) Hypothalamic involvement in Huntington's disease: an in vivo PET study. Brain: a journal of neurology 131: 2860-2869.
14. Hult S, Soylu R, Bjorklund T., Belgardt BF, Mauer J, et al. (2011) Mutant huntingtin causes metabolic imbalance by disruption of hypothalamic neurocircuits. Cell metabolism 13: 428-439.
15. Hult Lundh S., Nilsson N, Soylu R., Kirik D, Petersen A. (2013) Hypothalamic expression of mutant huntingtin contributes to the development of depressive-like behavior in the BAC transgenic mouse model of Huntington's disease. Hum Mol Genet 22: 3485-3497.
16. Gray M, Shirasaki DI, Cepeda C, Andre V.M., Wilburn B., et al. (2008) Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J Neurosci 28: 6182-6195.
17. Abada YS, Schreiber R, Ellenbroek B. (2013) Motor, emotional and cognitive deficits in adult BACHD mice: a model for Huntington's disease. Behav Brain Res 238: 243-251.
18. Lundh SH, Soylu R, Petersen A. (2012) Expression of mutant huntingtin in leptin receptor-expressing neurons does not control the metabolic and psychiatric phenotype of the BACHD mouse. PloS one 7: e51168.
19. Myers MG J.r., Olson D.P. (2012) Central nervous system control of metabolism. Nature 491: 357-363.
20. Bingham NC, Anderson KK, Reuter A.L., Stallings NR, Parker K.L. (2008) Selective loss of leptin receptors in the ventromedial hypothalamic nucleus results in increased adiposity and a metabolic syndrome. Endocrinology 149: 2138-2148.
21. Budefeld T, Tobet SA, Majdic G. (2012) Steroidogenic factor 1 and the central nervous system. J Neuroendocrinol 24: 225-235.
22. Ikeda Y, Takeda Y, Shikayama T., Mukai T, Hisano S, et al (2001) Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypotha-lamic-pituitary-gonadal axis suggests their closely related and distinct functions. Dev Dyn 220: 363-376.
23. Zhao L, Kim KW, Ikeda Y, Anderson K.K., Beck L., et al. (2008) Central nervous system-specific knockout of steroidogenic factor 1 results in increased anxiety-like behavior. Mol Endocrinol 22: 1403-1415.
24. McClellan KM, Parker KL, Tobet S. (2006) Development of the ventromedial nucleus of the hypothalamus. Front Neuroendocrinol 27: 193-209.
25. Cheung CC, Kurrasch DM, Liang J.K., Ingraham H.A. (2013) Genetic labeling of steroidogenic factor-1 (SF-1) neurons in mice reveals ventromedial nucleus of the hypothalamus (VMH) circuitry beginning at neurogenesis and development of a separate non-SF-1 neuronal cluster in the ventrolateral VMH. J Comp Neurol 521: 1268-1288.
26. Ikeda Y, Luo X, Abbud R., Nilson JH, Parker K.L. (1995) The nuclear receptor steroidogenic factor 1 is essential for the formation of the ventromedial hypothalamic nucleus. Mol Endocrinol 9: 478-486.
27. Dhillon H, Zigman JM, Ye C, Lee C.E., McGovern RA, et al. (2006) Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis. Neuron 49: 191-203.
28. Kim KW, Zhao L, Donato J Jr, Kohno D, Xu Y, et al (2011) Steroidogenic factor 1 directs programs regulating diet-induced thermogenesis and leptin action in the ventral medial hypothalamic nucleus. Proc Natl Acad Sci U S A 108: 10673-10678.
29. Kim KW, Jo YH, Zhao L, Stallings N.R., Chua SC Jr, et al. (2008) Steroidogenic factor 1 regulates expression of the cannabinoid receptor 1 in the ventromedial hypothalamic nucleus. Mol Endocrinol 22: 1950-1961.
30. Choi YH, Fujikawa T, Lee J., Reuter A, Kim K.W. (2013) Revisiting the Ventral Medial Nucleus of the Hypothalamus: The Roles of SF-1 Neurons in Energy Homeostasis. Front Neurosci 7: 71.
31. Pouladi MA, Xie Y, Skotte N.H., Ehrnhoefer DE, Graham RK, et al. (2010) Full-length huntingtin levels modulate body weight by influencing insulin-like growth factor 1 expression. Hum Mol Genet 19: 1528-1538.
32. Wang N, Gray M, Lu X.H., Cantle JP, Holley SM, et al. (2014) Neuronal targets for reducing mutant huntingtin expression to ameliorate disease in a mouse model of Huntington's disease. Nat Med 20: 536-541.
33. Walf AA, Frye C.A. (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2: 322-328.
34. Renoir T, Pang TY, Mo C, Chan G., Chevarin C, et al. (2013) Differential effects of early environmental enrichment on emotionality related behaviours in Huntington's disease transgenic mice. J Physiol 591: 41-55.
35. Porsolt RD, Bertin A, Jalfre M. (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229: 327-336.
36. Pouladi MA, Stanek LM, Xie Y, Franciosi S., Southwell AL, et al. (2012) Marked differences in neurochemistry and aggregates despite similar behavioural and neuropathological features of Huntington disease in the full-length BACHD and YAC128 mice. Hum Mol Genet 21: 2219-2232.
37. Parker KL, Rice DA, Lala D.S., Ikeda Y., Luo X, et al. (2002) Steroidogenic factor 1: an essential mediator of endocrine development. Recent Prog Horm Res 57: 19-36.
38. Kim KW, Sohn JW, Kohno D, Xu Y., Williams K, et al. (2011) SF-1 in the ventral medial hypothalamic nucleus: a key regulator of homeostasis. Mol Cell Endocrinol 336: 219-223.
39. Pla P, Orvoen S, Saudou F., David DJ, Humbert S. (2014) Mood disorders in Huntington's disease: from behavior to cellular and molecular mechanisms. Front Behav Neurosci 8: 135.
40. Pouladi MA, Morton AJ, Hayden M.R. (2013) Choosing an animal model for the study of Huntington's disease. Nat Rev Neurosci 14: 708-721.
41. Du X, Pang TY, Hannan A.J. (2013) A Tale of Two Maladies? Pathogenesis of Depression with and without the Huntington's Disease Gene Mutation. Front Neurol 4: 81.
42. Pang TY, Du X, Zajac M.S., Howard ML, Hannan A.J. (2009) Altered serotonin receptor expression is associated with depression-related behavior in the R6/1 transgenic mouse model of Huntington's disease. Hum Mol Genet 18: 753-766.
43. Van Raamsdonk J.M., 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.
44. Lloret A, Dragileva E, Teed A., Espinola J, Fossale E, et al (2006) Genetic background modifies nuclear mutant huntingtin accumulation and HD CAG repeat instability in Huntington's disease knock-in mice. Hum Mol Genet 15: 2015-2024.
45. 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.
46. Bueno CH, Zangrossi H Jr, Viana Mde B (2007) GABA/benzodiazepine receptors in the ventromedial hypothalamic nucleus regulate both anxiety and panic-related defensive responses in the elevated T-maze. Brain Res Bull 74: 134-141.
47. Canteras NS, Simerly RB, Swanson L.W. (1994) Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348: 41-79.
48. Suwanai AS, Ishii T, Haruna H., Yamataka A, Narumi S, et al (2013) A report of two novel NR5A1 mutation families: possible clinical phenotype of psychiatric symptoms of anxiety and/or depression. Clin Endocrinol (Oxf) 78: 957-965.
49. Hetherington AW, Ranson S.W. (1940) Hypothalamic lesions and adiposity in the rat. Anat Rec 78: 149-172.
50. Sakaguchi T, Arase K, Bray G.A. (1988) Sympathetic activity and food intake of rats with ventromedial hypothalamic lesions. Int J Obes 12: 285-291.
51. Rabin BM (1974) Independence of food intake and obesity following ventromedial hypothalamic lesions in the rat. Physiol Behav 13: 769-772.
52. Van Raamsdonk J.M., Gibson WT, Pearson J, Murphy Z., Lu G, et al. (2006) Body weight is modulated by levels of full-length huntingtin. Hum Mol Genet 15: 1513-1523.