Expression profile analysis of vulnerable CA1 pyramidal neurons in young-middle-aged Ts65Dn mice

Journal of Comparative Neurology

Volumn 523, Issue 1, 2015, Pages 61-74

  Alldred, Melissa J ^a,b   Lee, Sang Han ^a   Petkova, Eva ^a,b   Ginsberg, Stephen D ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; BDNF; Down syndrome; Hippocampus; Laser capture microdissection; Microarray; QPCR; RRID:AB_2314574, AB_397508, AB_2154265, AB_630940, AB_477580, AB_477262; RRID:IMSR_JAX:001924; TrkB; TrkC

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA1; ADVANCED GLYCATION END PRODUCT; BETA CATENIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CALSENILIN; CATALASE; CATECHOL METHYLTRANSFERASE; CATHEPSIN B; CYCLIN B1; CYCLIN D2; MYELIN BASIC PROTEIN; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; RNA; TRANSCRIPTOME;

AGE DISTRIBUTION; AGER GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAT GENE; CCNB1 GENE; CCND2 GENE; CHRNA2 GENE; COMT GENE; CONTROLLED STUDY; CTNNB1 GENE; CTSB GENE; DNA FINGERPRINTING; DOWN REGULATION; GABRA4 GENE; GABRD GENE; GABRG1 GENE; GENE; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GRM4 GENE; HIPPOCAMPAL CA1 REGION; HSPA5 GENE; IGFR1 GENE; IMMUNOBLOTTING; INVESTIGATIVE PROCEDURES; KCNIP3 GENE; LASER CAPTURE MICRODISSECTION; MAPT4 GENE; MBP GENE; MICROARRAY ANALYSIS; MOUSE; MOUSE STRAIN; MYO5B GENE; NERVE DEGENERATION; NONHUMAN; NPC2 GENE; NR4A3 GENE; NTRK2ECD GENE; NTRK3ECD GENE; NTRK3TK GENE; P75 GENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PTGS1 GENE; PYRAMIDAL NERVE CELL; RAB11A GENE; RAB9 GENE; REAL TIME POLYMERASE CHAIN REACTION; SAA4 GENE; SAPK3 GENE; SINGLE CELL ANALYSIS; TERMINAL CONTINUATION RNA AMPLIFICATION; TIMP1 GENE; TS65DN MOUSE; ANIMAL; DISEASE COURSE; DISEASE MODEL; DOWN SYNDROME; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOWN SYNDROME; FEMALE; IMMUNOBLOTTING; LASER CAPTURE MICRODISSECTION; MALE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; POLYMERASE CHAIN REACTION; PYRAMIDAL CELLS; TRANSCRIPTOME;

EID: 84909599287     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23663     Document Type: Article

References (89)

1. Akeson E, Lambert J. 2001. Ts65Dn-localization of the translocation breakpoint and trisomic gene content in a mouse model for Down syndrome. Cytogenet Cell Genet 276:270-276.
2. Alldred MJ, Che S, Ginsberg SD. 2008. Terminal continuation (TC) RNA amplification enables expression profiling using minute RNA input obtained from mouse brain. Int J Mol Sci 9:2091-2104.
3. Alldred MJ, Che S, Ginsberg SD. 2009. Terminal continuation (TC) RNA amplification without second strand synthesis. J Neurosci Methods 177:381-385.
4. Alldred MJ, Duff KE, Ginsberg SD. 2012. Microarray analysis of CA1 pyramidal neurons in a mouse model of tauopathy reveals progressive synaptic dysfunction. Neurobiol Dis 45:751-762.
5. Alldred MJ, Lee SH, Petkova E, Ginsberg SD. 2014. Expression profile analysis of hippocampal CA1 pyramidal neurons in aged Ts65Dn mice, a model of Down syndrome (DS) and Alzheimer's disease (AD). Brain Struct Funct, 2014 July 14 [Epub ahead of Print] DOI:10.1007/s00429-014-0839-0.
6. Applied Biosystems. 2008. Guide to performing relative quantitation of gene expression using real-time quantitative PCR. Gene Expr 2009:1-60.
7. Ash JA, Velazquez R, Kelley CM, Powers BE, Ginsberg SD, Mufson EJ, Strupp BJ. 2014. Maternal choline supplementation improves spatial mapping and increases basal forebrain cholinergic neuron number and size in aged Ts65Dn mice. Neurobiol Dis 70:32-42.
8. Belichenko PV, Masliah E, Kleschevnikov AM, Villar AJ, Epstein CJ, Salehi A, Mobley WC. 2004. Synaptic structural abnormalities in the Ts65Dn mouse model of Down syndrome. J Comp Neurol 480:281-298.
9. Belichenko NP, Belichenko PV, Kleschevnikov AM, Salehi A, Reeves RH, Mobley WC. 2009. The "Down syndrome critical region" is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. J Neurosci 29:5938-5948.
10. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289-300.
11. Blanchard J, Bolognin S, Chohan MO, Rabe A, Iqbal K, Gundke-Iqbal I. 2011. Rescue of synaptic failure and alleviation of learning and memory impairments in a trisomic mouse model of down syndrome. J Neuropathol Exp Neurol 70:1070-1079.
12. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, Nixon RA. 2000. Endocytic pathway abnormalities precede amyloid β deposition in sporadic Alzheimer's disease and Down syndrome. Am J Pathol 157:277-286.
13. Chao MV. 2003. Retrograde transport redux. Neuron 39:1-2.
14. Chapman R, Hesketh L. 2000. Behavioral phenotype of individuals with Down syndrome. Ment Retard Dev Disabil Res Rev 95:84-95.
15. Che S, Ginsberg SD. 2004. Amplification of RNA transcripts using terminal continuation. Lab Invest 84:131-137.
16. Chen Z, Simmons MS, Perry RT, Wiener HW, Harrell LE, Go RC. 2008. Genetic association of neurotrophic tyrosine kinase receptor type 2 (NTRK2) with Alzheimer's disease. Am J Med Genet B Neuropsychiatr Genet 147:363-369.
17. Chung B, Hinek A, Keating S, Weksberg R, Shah V, Blaser S, Hawlins C, Chitayat D. 2012. Overgrowth with increased proliferation of fibroblast and matrix metalloproteinase activity related to reduced TIMP1: a newly recognized syndrome? Am J Med Genet A 158A:2373-2381.
18. Contestabile A, Fila T, Bartesaghi R, Ciani E. 2006. Choline acetyltransferase activity at different ages in brain of Ts65Dn mice, an animal model for Down's syndrome and related neurodegenerative diseases. J Neurochem 97:515-526.
19. Cooper JD, Salehi A, Delcroix JD, Howe CL, Belichenko PV, Chua-Couzens J, Kilbridge JF, Carlson EJ, Epstein CJ, Mobley WC. 2001. Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc Natl Acad Sci U S A 98:10439-10444.
20. NTR) protein in early-stage Alzheimer's disease. Ann Neurol 56:520-531.
21. Counts SE, Che S, Ginsberg SD, Mufson EJ. 2011. Gender differences in neurotrophin and glutamate receptor expression in cholinergic nucleus basalis neurons during the progression of Alzheimer's disease. J Chem Neuroanat 42:111-117.
22. Counts SE, Alldred MJ, Che S, Ginsberg SD, Mufson EJ. 2014. Synaptic gene dysregulation within hippocampal CA1 pyramidal neurons in mild cognitive impairment. Neuropharmacology 79:172-179.
23. D'Alton S, George DR. 2011. Changing perspectives on Alzheimer's disease: thinking outside the amyloid box. J Alzheimers Dis 25:571-581.
24. Das I, Reeves RH. 2011. The use of mouse models to understand and improve cognitive deficits in Down syndrome. Dis Model Mech 4:596-606.
25. Davisson M, Schmidt C. 1993. Segmental trisomy as a mouse model for Down syndrome. Prog Clin Biol Res 117-133.
26. Efron B. 2007. Correlation and large-scale simultaneous significance testing. J Am Stat Assoc 102:93-103.
27. Esbensen AJ. 2010. Health conditions associated with aging and end of life of adults with Down syndrome. Int Rev Res Ment Retard 39:107-126.
28. Escorihuela RM, Fernández-Teruel A, Vallina IF, Baamonde C, Lumbreras MA, Dierssen M, Tobeña A, Flórez J. 1995. A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci Lett 199:143-146.
29. Fukuda Y, Berry TL, Nelson M, Hunter CC, Fukuhara K, Imai H, Ito S, Granhom-Bentley AC, Kaplan AP, Mutoh T. 2010. Stimulated neuronal expression of brain-derived neurotrophic factor by neurotropin. Mol Cell Neurosci 45:226-233.
30. Gardiner K, Fortna A, Bechtel L, Davisson MT. 2003. Mouse models of Down syndrome: how useful can they be? Comparison of the gene content of human chromosome 21 with orthologous mouse genomic regions. Gene 318:137-147.
31. Ginsberg SD. 2005a. Glutamatergic neurotransmission expression profiling in the mouse hippocampus after perforant-path transection. Am J Geriatr Pyschiatry 13:1052-1061.
32. Ginsberg SD. 2005b. RNA amplification strategies for small sample populations. Methods 37:229-237.
33. Ginsberg SD. 2007. Expression profile analysis of brain aging. In Riddle DR, editor. Brain aging: models, methods and mechanisms. New York, NY: CRC Press. pp 159-185.
34. Ginsberg SD. 2008. Transcriptional profiling of small samples in the central nervous system. Methods Mol Biol 439:147-158.
35. Ginsberg SD. 2009. Microarray use for the analysis of the CNS. In Squire LR, editor. Encyclopedia of neuroscience, vol. 5. Waltham, MA: Academic Press. pp 835-841.
36. Ginsberg SD. 2010. Alterations in discrete glutamate receptor subunits in adult mouse dentate gyrus granule cells following perforant path transection. Anal Bioanal Chem 397:3349-3358.
37. Ginsberg SD, Mirnics K. 2006. Functional genomic methodologies. Prog Brain Res 158:15-40.
38. Ginsberg SD, Hemby SE, Lee VMY, Eberwine JH, Trojanowski JQ. 2000. Expression profile of transcripts in Alzheimer's disease tangle-bearing CA1 neurons. Ann Neurol 48:77-87.
39. NTR gene expression in single cholinergic basal forebrain neurons mark the progression of Alzheimer's disease. J Neurochem 97:475-487.
40. Ginsberg SD, Alldred MJ, Counts SE, Cataldo AM, Neve RL, Jiang Y, Wuu J, Chao MV, Mufson EJ, Nixon RA, Che S. 2010a. Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biol Psychiatry 68:885-893.
41. Ginsberg SD, Mufson EJ, Counts SE, Wuu J, Aldred MJ, Nixon RA, Che S. 2010b. Regional selectivity of rab5 and rab7 protein upregulation in mild cognitive impairment and Alzheimer's disease. J Alzheimers Dis 22:631-639.
42. Ginsberg SD, Alldred MJ, Che S. 2012. Gene expression levels assessed by CA1 pyramidal neuron and regional hippocampal dissections in Alzheimer's disease. Neurobiol Dis 45:99-107.
43. 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.
44. Granholm A-C, Sanders L, Seo H, Lin L, Ford K, Isacson O. 2003. Estrogen alters amyloid precursor protein as well as dendritic and cholinergic markers in a mouse model of Down syndrome. Hippocampus 13:905-914.
45. Hanney M, Prasher V, Williams N, Jones EL, Aarsland D, Corbetta A, Lawrence D, Yu LM, Tyrer S, Francis PT, Johnson T, Bullock R, Ballard C; MEADOWS trial researchers. 2012. Memantine for dementia in adults older than 40 years with Down's syndrome (MEADOWS): a randomised, double-blind, placebo-controlled trial. Lancet 379:528-536.
46. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen K, Sun Y, Carlson E, Alleva E, Epstein CJ, Mobley WC. 1996. Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc Natl Acad Sci U S A 93:13333-13338.
47. Howe CL, Mobley WC. 2004. Signaling endosome hypothesis: a cellular mechanism for long distance communication. J Neurobiol 58:207-216.
48. Huang YZ, McNamara JO. 2012. Neuroprotective effects of reactive oxygen species mediated by BDNF-independent activation of TrkB. J Neurosci 32:15521-15532.
49. Hunter CL, Isacson O, Nelson M, Bimonte-Nelson H, Seo H, Lin L, Ford K, Kindy MS, Granholm AC. 2003. 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.
50. Hyde LA, Crnic LS. 2001. Age-related deficits in context discrimination learning in Ts65Dn mice that model Down syndrome and Alzheimer's disease. Behav Neurosci 115:1239-1246.
51. Insausti AM, Megías M, Crespo D, Cruz-Orive LM, Dierssen M, Vallina IF, Insausti R, Flórez J. 1998. Hippocampal volume and neuronal number in Ts65Dn mice: a murine model of Down syndrome. Neurosci Lett 253:175-178.
52. Jacobs PA, Hassold TJ. 1995. The origin of numerical chromosome abnormalities. Adv Genet 33:101-133.
53. Jiang Y, Mullaney KA, Peterhoff CM, Che S, Schmidt SD, Boyer-Boiteau A, Ginsberg SD, Cataldo AM, Mathews PM, Nixon RA. 2010. Alzheimer's-related endosome dysfunction in Down syndrome is Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc Natl Acad Sci U S A 107:1630-1635.
54. Kaur G, Sharma A, Xu W, Gerum S, Alldred MJ, Subhana 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.
55. Kelley C, Powers B, Velazquez R, Ash JA, Ginsberg SD, Strupp BJ, Mufson EJ. 2014a. Maternal choline supplementation differentially alters the basal forebrain cholinergic system of young-adult Ts65Dn and disomic mice. J Comp Neurol 522:1390-1410.
56. Kelley CM, Powers BE, Velazquez R, Ash JA, Ginsberg SD, Strupp BJ, Mufson EJ. 2014b. Sex differences in the cholinergic basal forebrain in the Ts65Dn mouse model of Down syndrome and Alzheimer's disease. Brain Pathol 24:33-44.
57. Kurt MA, Davies DC, Kidd M, Dierssen M, Flórez J. 2000. Synaptic deficit in the temporal cortex of partial trisomy 16 (Ts65Dn) mice. Brain Res 858:191-197.
58. Lane RF, Shineman DW, Steele JW, Lee LB, Fillit HM. 2012. Beyond amyloid: the future of therapeutics for Alzheimer's disease. Adv Pharmacol 64:213-271.
59. Lee VM, Carden MJ, Schlaepfer WW, Trojanowski JQ. 1987. Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J Neurosci 7:3474-3488.
60. Leverenz JB, Raskind MA. 1998. Early amyloid deposition in the medial temporal lobe of young Down syndrome patients: a regional quantitative analysis. Exp Neurol 150:296-304.
61. Levine S, Saltzman A, Levy E, Ginsberg SD. 2009. Systemic pathology in aged mouse models of Down's syndrome and Alzheimer's disease. Exp Mol Pathol 86:18-22.
62. Lockrow J, Prakasam A. 2009. Cholinergic degeneration and memory loss delayed by vitamin E in a Down syndrome mouse model. Exp Neurol 216:278-289.
63. Lorenzi HA, Reeves RH. 2006. Hippocampal hypocellularity in the Ts65Dn mouse originates early in development. Brain Res 1104:153-159.
64. Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH, Joung JK. 2013. CRISPR RNA-guided activation of endogenous human genes. Nat Methods 10:977-999.
65. Mann DM, Yates PO, Marcyniuk B, Ravindra CR. 1986. The topography of plaques and tangles in Down's syndrome patients of different ages. Neuropathol Appl Neurobiol 12:447-457.
66. McCulloch CE, Searle SR, Neuhaus JM. 2008. Generalized, linear, and mixed models. New York: John Wiley & Sons.
67. Moon J, Chen M, Gandhy SU, Strawderman M, Levitsky DA, Maclean KN, Strupp BJ. 2010. Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behav Neurosci 124:346-361.
68. Mufson EJ, Ginsberg SD, Ikonomovic MD, DeKosky ST. 2003. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J Chem Neuroanat 26:233-242.
69. Mufson EJ, Counts SE, Fahnestock M, Ginsberg SD. 2007. Cholinotrophic molecular substrates of mild cognitive impairment in the elderly. Curr Alzheimer Res 4:340-350.
70. Mufson EJ, Counts SE, Perez SE, Ginsberg SD. 2008. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 8:1703-1718.
71. Nixon RA, Cataldo AM. 2006. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J Alzheimers Dis 9:277-289.
72. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y, Meyer RE, Anderson P, Mason CA, Collins JS, Kirby RS, Correa A; National Birth Defects Prevention Network. 2010. Updated national birth prevalence estimates for selected birth defects in the United States, 2004-2006. Birth Defects Res A Clin Mol Teratol 88:1008-1016.
73. Peng S, Wuu J, Mufson EJ, Fahnestock M. 2005. Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J Neurochem 93:1412-1421.
74. Peng S, Garzon DJ, Marchese M, Klein W, Ginsberg SD, Francis BM, Mount HT, Mufson EJ, Salehi A, Fahnestock M. 2009. Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease. J Neurosci 29:9321-9329.
75. Pollonini G, Gao V, Rabe A, Palminiello S. 2008. Abnormal expression of synaptic proteins and neurotrophin-3 in the Down syndrome mouse model Ts65Dn. Neuroscience 156:99-106.
76. Rajagopal R, Chen Z-Y, Lee FS, Chao MV. 2004. Transactivation of Trk neurotrophin receptors by G-protein-coupled receptor ligands occurs on intracellular membranes. J Neurosci 24:6650-6658.
77. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, Schmidt C, Bronson RT, Davisson MT. 1995. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 11:177-184.
78. Rueda N, Flórez J, Martínez-Cué C. 2012. Mouse models of Down syndrome as a tool to unravel the causes of mental disabilities. Neural Plast 2012:584071.
79. Salehi A, Delcroix J-D, Belichenko PV, Zhan K, Wu C, Valleta 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.
80. Saran NG, Pletcher MT, Natale JE, Cheng Y, Reeves RH. 2003. Global disruption of the cerebellar transcriptome in a Down syndrome mouse model. Hum Mol Genet 12:2013-2019.
81. Seo H, Isacson O. 2005. Abnormal APP, cholinergic and cognitive function in Ts65Dn Down's model mice. Exp Neurol 193:469-480.
82. Skaper SD. 2008. The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol Disord Drug Targets 7:46-62.
83. Stempler S, Ruppin E. 2012. Analyzing gene expression from whole tissue vs. different cell types reveals the central role of neurons in predicting severity of Alzheimer's disease. PLoS One 7:e45879.
84. Sturgeon X, Gardiner KJ. 2011. Transcript catalogs of human chromosome 21 and orthologous chimpanzee and mouse regions. Mamm Genome 22:261-271.
85. Tuszynski M. 2002. Growth-factor gene therapy for neurodegenerative disorders. Lancet Neurol 1:51-57.
86. Tuszynski MH. 2007. Nerve growth factor gene therapy in Alzheimer disease. Alzheimer Dis Assoc Disord 21:179-189.
87. Velazquez R, Ash JA, Powers BE, Kelley CM, Strawderman M, Luscher ZI, Ginsberg SD, Mufson EJ, Strupp BJ. 2013. Maternal choline supplementation improves spatial learning and adult hippocampal neurogenesis in the Ts65Dn mouse model of Down syndrome. Neurobiol Dis 58:92-101.
88. Wisniewski K, Wisniewski H, Wen G. 1985. Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome. Ann Neurol 17:278-282.
89. Yan J, Ginsberg SD, Powers B, Alldred MJ, Saltzman A, Strupp BJ, Caudill MA. 2014. Maternal choline supplementation programs greater activity of the phosphatidylethanolamine N-methyltransferase (PEMT) pathway in adult Ts65Dn trisomic mice. FASEB J, 2104 Jun 24 [Epub ahead of Print] DOI:10.1096/FJ.14-251736.