Designer receptors enhance memory in a mouse model of down syndrome

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1343-1353

  Fortress, Ashley M ^a   Hamlett, Eric D ^a   Vazey, Elena M ^a   Aston Jones, Gary ^a   Cass, Wayne A ^c   Boger, Heather A ^a   Granholm, Ann Charlotte E ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Designer receptors; Down syndrome; Hippocampus; Locus coeruleus; Neurodegeneration; Noradrenergic

Indexed keywords

AMYLOID PROTEIN; BETA 1 ADRENERGIC RECEPTOR; CLOZAPINE N OXIDE; DESIGNER DRUG; DESIGNER RECEPTORS EXCLUSIVELY ACTIVATED BY DESIGNER DRUG; DROXIDOPA; NORADRENALIN; UNCLASSIFIED DRUG; 3-(4-(METHYLTHIO)PHENYLSERINE); CLOZAPINE; CLOZAPINE N-OXIDE; MUSCARINIC M3 RECEPTOR; NEUROLEPTIC AGENT; SERINE;

ADENO ASSOCIATED VIRUS; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION; BEHAVIOR; CELL COUNTING; CONTROLLED STUDY; DEMENTIA; DENSITOMETRY; DISEASE COURSE; DOWN SYNDROME; EXECUTIVE FUNCTION; FLUORESCENCE MICROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HYPERACTIVITY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LOCOMOTION; LOCUS CERULEUS; MALE; MEMORY; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; NORADRENERGIC SYSTEM; NOVEL OBJECT RECOGNITION TEST; OXIDATIVE STRESS; PRIORITY JOURNAL; WORKING MEMORY; ANALOGS AND DERIVATIVES; ANIMAL; CELL COUNT; COMPLICATION; CROSSOVER PROCEDURE; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MAZE TEST; MEMORY DISORDERS; METABOLISM; MOTOR ACTIVITY; MOUSE MUTANT; NEURODEGENERATIVE DISEASES; PATHOLOGY; PHYSIOLOGY; RADIATION RESPONSE;

ANIMALS; ANTIPSYCHOTIC AGENTS; CELL COUNT; CLOZAPINE; CROSS-OVER STUDIES; DESIGNER DRUGS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; HUMANS; LOCUS COERULEUS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, NEUROLOGIC MUTANTS; MOTOR ACTIVITY; NEURODEGENERATIVE DISEASES; RECEPTOR, MUSCARINIC M3; SERINE;

EID: 84921930781     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2658-14.2015     Document Type: Article

References (59)

1. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA, Nonneman RJ, Hartmann J, Moy SS, Nicolelis MA, McNamara JO, Roth BL (2009) Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63:27-39. CrossRef Medline
2. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL (2007) Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A 104:5163-5168. CrossRef Medline
3. Boger HA, Middaugh LD, Huang P, Zaman V, Smith AC, Hoffer BJ, Tomac AC, Granholm AC (2006) A partial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Exp Neurol 202:336-347. CrossRef Medline
4. Boger HA, Mannangatti P, Samuvel DJ, Saylor AJ, Bender TS, McGinty JF, Fortress AM, Zaman V, Huang P, Middaugh LD, Randall PK, Jayanthi LD, Rohrer B, Helke KL, Granholm AC, Ramamoorthy S (2011) Effects of brain-derived neurotrophic factor on dopaminergic function and motor behavior during aging. Genes Brain Behav 10:186-198. CrossRef Medline
5. Bramham CR, Bacher-Svendsen K, Sarvey JM (1997) LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport 8:719-724. CrossRef Medline
6. Cass WA, Harned ME, Peters LE, Nath A, Maragos WF (2003) HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res 984:133-142. CrossRef Medline
7. Chalermpalanupap T, Kinkead B, Hu WT, Kummer MP, Hammerschmidt T, Heneka MT, Weinshenker D, Levey AI (2013) Targeting norepineph-rine in mild cognitive impairment and Alzheimer’s disease. Alzheimers Res Ther 5:21. CrossRef Medline
8. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853-8860. Medline
9. Dang V, Medina B, Das D, Moghadam S, Martin KJ, Lin B, Naik P, Patel D, Nosheny R, Wesson Ashford J, Salehi A (2014) Formoterol, a longacting β2 adrenergic agonist, improves cognitive function and promotes dendritic complexity in a mouse model of Down syndrome. Biol Psychiatry 75:179-188. CrossRef Medline
10. Davisson MT, Schmidt C, Akeson EC (1990) Segmental trisomy of murine chromosome 16: a new model system for studying Down syndrome. Prog Clin Biol Res 360:263-280. Medline
11. Escorihuela RM, Fernández-Teruel A, Vallina IF, Baamonde C, Lumbreras MA, Dierssen M, Tobenã A, Flórez J (1995) A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci Lett 199:143-146. CrossRef Medline
12. German DC, Manaye KF, White CL III, Woodward DJ, McIntire DD, Smith WK, Kalaria RN, Mann DM (1992) Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 32:667-676. CrossRef Medline
13. Glasson EJ, Dye DE, Bittles AH (2014) The triple challenges associated with age-related comorbidities in Down syndrome. J Intellect Disabil Res 58: 393-398. CrossRef Medline
14. Granholm AC, Sanders LA, Crnic LS (2000) Loss of cholinergic phenotype in basal forebrain coincides with cognitive decline in a mouse model of Down’s syndrome. Exp Neurol 161:647-663. CrossRef Medline
15. Hammerschmidt T, Kummer MP, Terwel D, Martinez A, Gorji A, Pape HC, Rommelfanger KS, Schroeder JP, Stoll M, Schultze J, Weinshenker D, Heneka MT (2013) Selective loss of noradrenaline exacerbates early cognitive dysfunction and synaptic deficits in APP/PS1 mice. Biol Psychiatry 73:454-463. CrossRef Medline
16. Head E, Garzon-Rodriguez W, Johnson JK, Lott IT, Cotman CW, Glabe C (2001) Oxidation of Abeta and plaque biogenesis in Alzheimer’s disease and Down syndrome. Neurobiol Dis 8:792-806. CrossRef Medline
17. Hunter CL, Bimonte HA, Granholm AC (2003a) Behavioral comparison of 4 and 6 month-old Ts65Dn mice: age-related impairments in working and reference memory. Behav Brain Res 138:121-131. CrossRef Medline
18. Hunter CL, Isacson O, Nelson M, Bimonte-Nelson H, Seo H, Lin L, Ford K, Kindy MS, Granholm AC (2003b) Regional alterations in amyloid precursor protein and nerve growth factor across age in a mouse model of Down’s syndrome. Neurosci Res 45:437-445. CrossRef Medline
19. Hunter CL, Bachman D, Granholm AC (2004) Minocycline prevents cholinergic loss in a mouse model of Down’s syndrome. Ann Neurol 56:675-688. CrossRef Medline
20. Hwang DY, Carlezon WA Jr, Isacson O, Kim KS (2001) A high-efficiency synthetic promoter that drives transgene expression selectively in noradrenergic neurons. Hum Gene Ther 12:1731-1740. CrossRef Medline
21. Isaacson SH, Skettini J (2014) Neurogenic orthostatic hypotension in Parkinson’s disease: evaluation, management, and emerging role of droxidopa. Vasc Health Risk Manag 10:169-176. CrossRef Medline
22. Iulita MF, Do Carmo S, Ower AK, Fortress AM, Aguilar LF, Hanna M, Wisniewski T, Granholm AC, Buhusi M, Busciglio J, Cuello AC (2014) Nerve growth factor metabolic dysfunction in Down’s syndrome brains. Brain 137:860-872. CrossRef Medline
23. Kalinin S, Gavrilyuk V, Polak PE, Vasser R, Zhao J, Heneka MT, Feinstein DL (2007) Noradrenaline deficiency in brain increases beta-amyloid plaque burden in an animal model of Alzheimer’s disease. Neurobiol Aging 28: 1206-1214. CrossRef Medline
24. Kato T, Karai N, Katsuyama M, Nakamura M, Katsube J (1987) Studies on the activity of L-threo-3,4-dihydroxyphenylserine (L-DOPS) as a catecholamine precursor in the brain. Comparison with that of L-dopa. Biochem Pharmacol 36:3051-3057. CrossRef Medline
25. Kaur G, Sharma A, Xu W, Gerum S, Alldred MJ, Subbanna S, Basavarajappa BS, Pawlik M, Ohno M, Ginsberg SD, Wilson DA, Guilfoyle DN, Levy E (2014) Glutamatergic transmission aberration: a major cause of behavioral deficits in a murine model of Down’s syndrome. J Neurosci 34: 5099-5106. CrossRef Medline
26. Kittler PM, Krinsky-McHale SJ, Devenny DA (2008) Dual-task processing as a measure of executive function: a comparison between adults with Williams and Down syndromes. Am J Ment Retard 113:117-132. CrossRef Medline
27. Krinsky-McHale SJ, Devenny DA, Kittler P, Silverman W (2008) Selective attention deficits associated with mild cognitive impairment and early stage Alzheimer’s disease in adults with Down syndrome. Am J Ment Retard 113:369-386. CrossRef Medline
28. Lanfranchi S, Jerman O, Dal Pont E, Alberti A, Vianello R (2010) Executive function in adolescents with Down syndrome. J Intellect Disabil Res 54: 308-319. CrossRef Medline
29. Lockrow JP, Fortress AM, Granholm AC (2012) Age-related neurodegeneration and memory loss in down syndrome. Curr Gerontol Geriatr Res 2012:463909. CrossRef Medline
30. Lockrow J, Prakasam A, Huang P, Bimonte-Nelson H, Sambamurti K, Granholm AC (2009) Cholinergic degeneration and memory loss delayed by vitamin E in a Down syndrome mouse model. Exp Neurol 216:278-289. CrossRef Medline
31. Lockrow J, Boger H, Bimonte-Nelson H, Granholm AC (2011) Effects of long-term memantine on memory and neuropathology in Ts65Dn mice, a model for Down syndrome. Behav Brain Res 221:610-622. CrossRef Medline
32. Lockrow J, Boger H, Gerhardt G, Aston-Jones G, Bachman D, Granholm AC (2011) A noradrenergic lesion exacerbates neurodegeneration in a Down syndrome mouse model. J Alzheimers Dis 23:471-489. CrossRef Medline
33. Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189:699-710. CrossRef Medline
34. Mann DM, Yates PO, Marcyniuk B (1986) Acomparison of nerve cell loss in cortical and subcortical structures in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 49:310-312. CrossRef Medline
35. Morris RG (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829-2846. CrossRef Medline
36. Murchison CF, Zhang XY, Zhang WP, Ouyang M, Lee A, Thomas SA (2004) A distinct role for norepinephrine in memory retrieval. Cell 117:131-143. CrossRef Medline
37. Murchison CF, Schutsky K, Jin SH, Thomas SA (2011) Norepinephrine and ss(1)-adrenergic signaling facilitate activation of hippocampal CA1 pyramidal neurons during contextual memory retrieval. Neuroscience 181: 109-116. CrossRef Medline
38. Nawaratne V, Leach K, Suratman N, Loiacono RE, Felder CC, Armbruster BN, Roth BL, Sexton PM, Christopoulos A (2008) New insights into the function of M4 muscarinic acetylcholine receptors gained using a novel allosteric modulator and a DREADD (designer receptor exclusively activated by a designer drug). Mol Pharmacol 74:1119-1131. CrossRef Medline
39. Nelson L, Johnson JK, Freedman M, Lott I, Groot J, Chang M, Milgram NW, Head E (2005) Learning and memory as a function of age in Down syndrome: a study using animal-based tasks. Prog Neuropsychopharmacol Biol Psychiatry 29:443-453. CrossRef Medline
40. O’Donnell J, Zeppenfeld D, McConnell E, Pena S, Nedergaard M (2012) Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem Res 37:2496-2512. CrossRef Medline
41. Ouyang M, Thomas SA (2005) A requirement for memory retrieval during and after long-term extinction learning. Proc Natl Acad Sci U S A 102: 9347-9352. CrossRef Medline
42. Paxinos G, Franklin K (2004) The mouse brain in stereotaxic coordinates. San Diego, CA: Academic
43. Pei Y, Dong S, Roth BL (2010) Generation of designer receptors exclusively activated by designer drugs (DREADDs) using directed molecular evolution. Curr Protoc Neurosci Chapter 4:Unit 4.33. CrossRef Medline
44. Ragozzino ME, Pal SN, Unick K, Stefani MR, Gold PE (1998) Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. J Neurosci 18:1595-1601. Medline
45. Ruparelia A, Pearn ML, Mobley WC (2013) Aging and intellectual disability: insights from mouse models of Down syndrome. Dev Disabil Res Rev 18:43-50. CrossRef Medline
46. Salehi A, Delcroix JD, Belichenko PV, Zhan K, Wu C, Valletta JS, Takimoto-Kimura R, Kleschevnikov AM, Sambamurti K, Chung PP, Xia W, Villar A, Campbell WA, Kulnane LS, Nixon RA, Lamb BT, Epstein CJ, Stokin GB, Goldstein LS, Mobley WC (2006) Increased App expression in a mouse model of Down’s syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 51:29-42. CrossRef Medline
47. Salehi A, Faizi M, Colas D, Valletta J, Laguna J, Takimoto-Kimura R, Kleschevnikov A, Wagner SL, Aisen P, Shamloo M, Mobley WC (2009) Restoration of norepinephrine-modulated contextual memory in a mouse model of Down syndrome. Sci Transl Med 1:7ra17. CrossRef
48. Savage LM, Chang Q, Gold PE (2003) Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learn Mem 10:242-246. CrossRef Medline
49. Schliebs R, Arendt T (2011) The cholinergic system in aging and neuronal degeneration. Behav Brain Res 221:555-563. CrossRef Medline
50. Stanton PK, Sarvey JM (1985) Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J Neurosci 5:2169-2176. Medline
51. Stefani MR, Gold PE (2001) Intrahippocampal infusions of k-ATP channel modulators influence spontaneous alternation performance: relationships to acetylcholine release in the hippocampus. J Neurosci 21:609-614. Medline
52. Stoltzner SE, Grenfell TJ, Mori C, Wisniewski KE, Wisniewski TM, Selkoe DJ, Lemere CA (2000) Temporal accrual of complement proteins in amyloid plaques in Down’s syndrome with Alzheimer’s disease. Am J Pathol 156:489-499. CrossRef Medline
53. Thomas SA, Palmiter RD (1997) Disruption of the dopamine betahydroxylase gene in mice suggests roles for norepinephrine in motor function, learning, and memory. Behav Neurosci 111:579-589. CrossRef Medline
54. Vazey EM, Aston-Jones G (2012) The emerging role of norepinephrine in cognitive dysfunctions of Parkinson’s disease. Front Behav Neurosci 6:48. CrossRef Medline
55. Vazey EM, Aston-Jones G (2014) Designer receptor manipulations reveal a role of the locus coeruleus noradrenergic system in isoflurane general anesthesia. Proc Natl Acad Sci U S A 111:3859-3864. CrossRef Medline
56. Warner G, Moss J, Smith P, Howlin P (2014) Autism characteristics and behavioural disturbances in β500 children with Down’s syndrome in England and Wales. Autism Res 7:433-441. CrossRef Medline
57. Wisniewski KE, Wisniewski HM, Wen GY (1985) Occurrence of neuropathological changes and dementia of Alzheimer’s disease in Down’s syndrome. Ann Neurol 17:278-282. CrossRef Medline
58. Zhang L, Ouyang M, Ganellin CR, Thomas SA (2013) The slow afterhyperpolarization: a target of β1-adrenergic signaling in hippocampusdependent memory retrieval. J Neurosci 33:5006-5016. CrossRef Medline
59. Zigman WB (2013) Atypical aging in Down syndrome. Dev Disabil Res Rev 18:51-67. CrossRef Medline