Neurobiological elements of cognitive dysfunction in down syndrome: Exploring the role of APP

Biological Psychiatry

Volumn 71, Issue 5, 2012, Pages 403-409

  Millan Sanchez, Martha ^a,b   Heyn, Sietske N ^a,b   Das, Devsmita ^a,b   Moghadam, Sarah ^a,b   Martin, Kara J ^a,b   Salehi, Ahmad ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Down syndrome; L DOPS; locus coeruleus; mouse models; norepinephrine; Ts65Dn mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CARBIDOPA; THREO 3,4 DIHYDROXYPHENYLSERINE;

CHOLINERGIC SYSTEM; COGNITIVE DEFECT; DEGENERATION; DOWN SYNDROME; EXPERIMENTAL MODEL; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; MOLECULAR MECHANICS; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; REVIEW;

ADRENERGIC NEURONS; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CHOLINERGIC NEURONS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; HUMANS;

EID: 84858380551     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.08.016     Document Type: Review

References (94)

1. A. Salehi, B. Pohlman, W.C. Mobley Down Syndrome/Trisomy 21 L.R. Squire, The New Encyclopedia of Neuroscience 2008 Elsevier San Diego
2. K.E. Wisniewski, H.M. Wisniewski, G.Y. Wen Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome Ann Neurol 17 1985 278 282 (Pubitemid 15136603)
3. F. Lai, R.S. Williams A prospective study of Alzheimer disease in Down syndrome Arch Neurol 46 1989 849 853 (Pubitemid 19199367)
4. M.A. Melyn, D.T. White Mental and developmental milestones of noninstitutionalized Down's syndrome children Pediatrics 52 1973 542 545
5. A. Shanks, A. Odibo Nasal bone in prenatal trisomy 21 screening Obstet Gynecol Surv 65 2010 46 52
6. G. Kanamori, M. Witter, J. Brown, L. Williams-Smith Otolaryngologic manifestations of Down syndrome Otolaryngol Clin North Am 33 2000 1285 1292 (Pubitemid 32060509)
7. M.S. Siegel, W.E. Smith Psychiatric features in children with genetic syndromes: Toward functional phenotypes Child Adolesc Psychiatr Clin N Am 19 2010 229 261 viii
8. B. Kallen, P. Mastroiacovo, E. Robert Major congenital malformations in Down syndrome Am J Med Genet 65 1996 160 166
9. N.J. Roizen, M.B. Mets, T.A. Blondis Ophthalmic disorders in children with Down syndrome Dev Med Child Neurol 36 1994 594 600 (Pubitemid 24182765)
10. S.B. Freeman, L.H. Bean, E.G. Allen, S.W. Tinker, A.E. Locke, C. Druschel Ethnicity, sex, and the incidence of congenital heart defects: A report from the National Down Syndrome Project Genet Med 10 2008 173 180 (Pubitemid 351416813)
11. R.A. Morrison, A. McGrath, G. Davidson, J.J. Brown, G.D. Murray, A.F. Lever Low blood pressure in Down's syndrome, A link with Alzheimer's disease? Hypertension 28 1996 569 575 (Pubitemid 26327951)
12. C.T. Fong, G.M. Brodeur Down's syndrome and leukemia: Epidemiology, genetics, cytogenetics and mechanisms of leukemogenesis Cancer Genet Cytogenet 28 1987 55 76 (Pubitemid 17153555)
13. J.D. Rowley Down Syndrome and acute leukaemia: Increased risk may be due to trisomy 21 Lancet 2 1981 1020 1022 (Pubitemid 11027580)
14. W.I. Cohen Current dilemmas in Down syndrome clinical care: Celiac disease, thyroid disorders, and atlanto-axial instability Am J Med Genet C Semin Med Genet 142C 2006 141 148 (Pubitemid 44298196)
15. T.C. Hankinson, R.C. Anderson Craniovertebral junction abnormalities in Down syndrome Neurosurgery 66 2010 32 38
16. Y. Hawli, M.El-Hajj Fuleihan G. Nasrallah Endocrine and musculoskeletal abnormalities in patients with Down syndrome Nat Rev Endocrinol 5 2009 327 334
17. H. Goldberg-Stern, R.H. Strawsburg, B. Patterson, F. Hickey, M. Bare, N. Gadoth Seizure frequency and characteristics in children with Down syndrome Brain Dev 23 2001 375 378 (Pubitemid 32913053)
18. M.E. Dyken, D.C. Lin-Dyken, S. Poulton, M.B. Zimmerman, E. Sedars Prospective polysomnographic analysis of obstructive sleep apnea in down syndrome Arch Pediatr Adolesc Med 157 2003 655 660 (Pubitemid 36818645)
19. D.K. Ng, H.N. Hui, C.H. Chan, K.L. Kwok, P.Y. Chow, J.M. Cheung Obstructive sleep apnoea in children with Down syndrome Singapore Med J 47 2006 774 779 (Pubitemid 44378776)
20. S.R. Shott Down syndrome: Common otolaryngologic manifestations Am J Med Genet C Semin Med Genet 142C 2006 131 140 (Pubitemid 44298195)
21. N. Schupf, D. Kapell, J.H. Lee, W. Zigman, B. Canto, B. Tycko Onset of dementia is associated with apolipoprotein E epsilon4 in Down's syndrome Ann Neurol 40 1996 799 801 (Pubitemid 26415194)
22. J. Krmpotic-Nemanic Down's syndrome and presbyacousis Lancet 2 1970 670 671
23. N.J. Roizen, C. Wolters, T. Nicol, T.A. Blondis Hearing loss in children with Down syndrome J Pediatr 123 1993 S9 S12
24. G. Miolo, R.S. Chapman, H.A. Sindberg Sentence comprehension in adolescents with Down syndrome and typically developing children: Role of sentence voice, visual context, and auditory-verbal short-term memory J Speech Lang Hear Res 48 2005 172 188 (Pubitemid 40470881)
25. G. Bhagyalakshmi, A.J. Renukarya, S. Rajangam Metric analysis of the hard palate in children with Down syndrome: A comparative study Downs Syndr Res Pract 12 2007 55 59
26. R.S. Chapman, L.J. Hesketh Behavioral phenotype of individuals with Down syndrome Ment Retard Dev Disabil Res Rev 6 2000 84 95 (Pubitemid 30399531)
27. L.J. Hesketh, R.S. Chapman Verb use by individuals with Down syndrome Am J Ment Retard 103 1998 288 304 (Pubitemid 29393707)
28. C. Jarrold, A.D. Baddeley Short-term memory in Down syndrome: Applying the working memory model Downs Syndr Res Pract 7 2001 17 23
29. J.O. Edgin, B.F. Pennington, C.B. Mervis Neuropsychological components of intellectual disability: The contributions of immediate, working, and associative memory J Intellect Disabil Res 54 2010 406 417
30. B.A. Myers, S.M. Pueschel Psychiatric disorders in persons with Down syndrome J Nerv Ment Dis 179 1991 609 613
31. A. Gath, D. Gumley Behaviour problems in retarded children with special reference to Down's syndrome Br J Psychiatry 149 1986 156 161 (Pubitemid 16076248)
32. L. Kent, J. Evans, M. Paul, M. Sharp Comorbidity of autistic spectrum disorders in children with Down syndrome Dev Med Child Neurol 41 1999 153 158 (Pubitemid 29127085)
33. F. Tyrer, C.W. McGrother, C.F. Thorp, M. Donaldson, S. Bhaumik, J.M. Watson Physical aggression towards others in adults with learning disabilities: Prevalence and associated factors J Intellect Disabil Res 50 2006 295 304 (Pubitemid 43329507)
34. R.A. Collacott, S.A. Cooper, C. McGrother Differential rates of psychiatric disorders in adults with Down's syndrome compared with other mentally handicapped adults Br J Psychiatry 161 1992 671 674
35. T. Maatta, T. Tervo-Maatta, A. Taanila, M. Kaski, M. Iivanainen Mental health, behaviour and intellectual abilities of people with Down syndrome Downs Syndr Res Pract 11 2006 37 43
36. D.M. Mann, M.M. Esiri The pattern of acquisition of plaques and tangles in the brains of patients under 50 years of age with Down's syndrome J Neurol Sci 89 1989 169 179 (Pubitemid 19052948)
37. N. Schupf, G.H. Sergievsky Genetic and host factors for dementia in Down's syndrome Br J Psychiatry 180 2002 405 410 (Pubitemid 34499334)
38. J.D. Pinter, S. Eliez, J.E. Schmitt, G.T. Capone, A.L. Reiss Neuroanatomy of Down's syndrome: A high-resolution MRI study Am J Psychiatry 158 2001 1659 1665 (Pubitemid 32923659)
39. J.D. Pinter, W.E. Brown, S. Eliez, J.E. Schmitt, G.T. Capone, A.L. Reiss Amygdala and hippocampal volumes in children with Down syndrome: A high-resolution MRI study Neurology 56 2001 972 974 (Pubitemid 32290819)
40. N.S. White, M.T. Alkire, R.J. Haier A voxel-based morphometric study of nondemented adults with Down Syndrome Neuroimage 20 2003 393 403 (Pubitemid 37188527)
41. S.J. Teipel, G.E. Alexander, M.B. Schapiro, H.J. Moller, S.I. Rapoport, H. Hampel Age-related cortical grey matter reductions in non-demented Down's syndrome adults determined by MRI with voxel-based morphometry Brain 127 2004 811 824 (Pubitemid 38478526)
42. R. Weitzdoerfer, M. Dierssen, M. Fountoulakis, G. Lubec Fetal life in Down syndrome starts with normal neuronal density but impaired dendritic spines and synaptosomal structure J Neural Transm Suppl 2001 59 70 (Pubitemid 38085072)
43. M. Marin-Padilla Pyramidal cell abnormalities in the motor cortex of a child with Down's syndrome A Golgi study J Comp Neurol 167 1976 63 81
44. S. Takashima, A. Ieshima, H. Nakamura, L.E. Becker Dendrites, dementia and the Down syndrome Brain Dev 11 1989 131 133 (Pubitemid 19106477)
45. I. Ferrer, F. Gullotta Down's syndrome and Alzheimer's disease: Dendritic spine counts in the hippocampus Acta Neuropathol 79 1990 680 685 (Pubitemid 20170346)
46. E.C. Downes, J. Robson, E. Grailly, Z. Abdel-All, J. Xuereb, C. Brayne Loss of synaptophysin and synaptosomal-associated protein 25-kDa (SNAP-25) in elderly Down syndrome individuals Neuropathol Appl Neurobiol 34 2008 12 22
47. M. Sadowski, H.M. Wisniewski, M. Tarnawski, P.B. Kozlowski, B. Lach, J. Wegiel Entorhinal cortex of aged subjects with Down's syndrome shows severe neuronal loss caused by neurofibrillary pathology Acta Neuropathol 97 1999 156 164 (Pubitemid 29134544)
48. P.R. Hof, C. Bouras, D.P. Perl, D.L. Sparks, N. Mehta, J.H. Morrison Age-related distribution of neuropathologic changes in the cerebral cortex of patients with Down's syndrome Quantitative regional analysis and comparison with Alzheimer's disease Arch Neurol 52 1995 379 391
49. A. Goate, M.C. Chartier-Harlin, M. Mullan, J. Brown, F. Crawford, L. Fidani Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease Nature 349 1991 704 706 (Pubitemid 21912142)
50. A. Rovelet-Lecrux, D. Hannequin, G. Raux, N. Le Meur, A. Laquerriere, A. Vital APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy Nat Genet 38 2006 24 26 (Pubitemid 43011878)
51. V.P. Prasher, M.J. Farrer, A.M. Kessling, E.M. Fisher, R.J. West, P.C. Barber Molecular mapping of Alzheimer-type dementia in Down's syndrome Ann Neurol 43 1998 380 383 (Pubitemid 28113601)
52. A. Salehi, J.D. Delcroix, P.V. Belichenko, K. Zhan, C. Wu, J.S. Valletta Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration Neuron 51 2006 29 42 (Pubitemid 43963336)
53. F. Acquati, M. Accarino, C. Nucci, P. Fumagalli, L. Jovine, S. Ottolenghi The gene encoding DRAP (BACE2), a glycosylated transmembrane protein of the aspartic protease family, maps to the down critical region FEBS Lett 468 2000 59 64 (Pubitemid 30101682)
54. K. Liu, I. Solano, D. Mann, C. Lemere, M. Mercken, J.Q. Trojanowski Characterization of Abeta11-40/42 peptide deposition in Alzheimer's disease and young Down's syndrome brains: Implication of N-terminally truncated Abeta species in the pathogenesis of Alzheimer's disease Acta Neuropathol 112 2006 163 174
55. X. Sun, G. He, W. Song BACE2, as a novel APP theta-secretase, is not responsible for the pathogenesis of Alzheimer's disease in Down syndrome FASEB J 20 2006 1369 1376 (Pubitemid 44943845)
56. A. Salehi, M. Faizi, D. Colas, J. Valletta, J. Laguna, R. Takimoto-Kimura Restoration of norepinephrine-modulated contextual memory in a mouse model of Down syndrome Sci Transl Med 1 2009 7ra17
57. C.L. Hunter, H.A. Bimonte, A.C. Granholm Behavioral comparison of 4 and 6 month-old Ts65Dn mice: Age-related impairments in working and reference memory Behav Brain Res 138 2003 121 131 (Pubitemid 36071351)
58. F. Fernandez, W. Morishita, E. Zuniga, J. Nguyen, M. Blank, R.C. Malenka Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome Nat Neurosci 10 2007 411 413 (Pubitemid 46494581)
59. H.A. Lorenzi, R.H. Reeves Hippocampal hypocellularity in the Ts65Dn mouse originates early in development Brain Res 1104 2006 153 159 (Pubitemid 44148518)
60. J.E. Hanson, M. Blank, R.A. Valenzuela, C.C. Garner, D.V. Madison The functional nature of synaptic circuitry is altered in area CA3 of the hippocampus in a mouse model of Down's syndrome J Physiol 579 2007 53 67
61. P.V. Belichenko, E. Masliah, A.M. Kleschevnikov, A.J. Villar, C.J. Epstein, A. Salehi Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome J Comp Neurol 480 2004 281 298 (Pubitemid 39578025)
62. P.V. Belichenko, A.M. Kleschevnikov, E. Masliah, C. Wu, R. Takimoto-Kimura, A. Salehi Excitatory-inhibitory relationship in the fascia dentata in the Ts65Dn mouse model of Down syndrome J Comp Neurol 512 2009 453 466
63. A. Easton, A.E. Fitchett, M.J. Eacott, M.G. Baxter Medial septal cholinergic neurons are necessary for context-place memory but not episodic-like memory Hippocampus 21 2010 1021 1027
64. E.G. McGeer, M. Norman, B. Boyes, J. O'Kusky, J. Suzuki, P.L. McGeer Acetylcholine and aromatic amine systems in postmortem brain of an infant with Down's syndrome Exp Neurol 87 1985 557 570 (Pubitemid 15144765)
65. M.F. Casanova, L.C. Walker, P.J. Whitehouse, D.L. Price Abnormalities of the nucleus basalis in Down's syndrome Ann Neurol 18 1985 310 313 (Pubitemid 15023103)
66. D.M. Mann, P.O. Yates, B. Marcyniuk Alzheimer's presenile dementia, senile dementia of Alzheimer type and Down's syndrome in middle age form an age related continuum of pathological changes Neuropathol Appl Neurobiol 10 1984 185 207 (Pubitemid 14121330)
67. I.T. Lott, K. Osann, E. Doran, L. Nelson Down syndrome and Alzheimer disease: Response to donepezil Arch Neurol 59 2002 1133 1136 (Pubitemid 34755826)
68. J.H. Heller, G.A. Spiridigliozzi, J.A. Sullivan, P.M. Doraiswamy, R.R. Krishnan, P.S. Kishnani Donepezil for the treatment of language deficits in adults with Down syndrome: A preliminary 24-week open trial Am J Med Genet A 116A 2003 111 116 (Pubitemid 36043380)
69. T. Kondoh, A. Kanno, H. Itoh, M. Nakashima, R. Honda, M. Kojima Donepezil significantly improves abilities in daily lives of female Down syndrome patients with severe cognitive impairment: A 24-week randomized, double-blind, placebo-controlled trial Int J Psychiatry Med 41 2011 71 89
70. J.D. Cooper, A. Salehi, J.D. Delcroix, C.L. Howe, P.V. Belichenko, J. Chua-Couzens 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 2001 10439 10444 (Pubitemid 32803038)
71. A. Salehi, J.D. Delcroix, D.F. Swaab Alzheimer's disease and NGF signaling J Neural Transm 111 2004 323 345 (Pubitemid 38316609)
72. A. Salehi, J.D. Delcroix, W.C. Mobley Traffic at the intersection of neurotrophic factor signaling and neurodegeneration Trends Neurosci 26 2003 73 80 (Pubitemid 36110541)
73. T.J. Sendera, S.Y. Ma, S. Jaffar, P.B. Kozlowski, J.H. Kordower, Y. Mawal Reduction in TrkA-immunoreactive neurons is not associated with an overexpression of galaninergic fibers within the nucleus basalis in Down's syndrome J Neurochem 74 2000 1185 1196 (Pubitemid 30104316)
74. Y. Jiang, K.A. Mullaney, C.M. Peterhoff, S. Che, S.D. Schmidt, A. Boyer-Boiteau 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 2010 1630 1635
75. R.A. Nixon Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases Neurobiol Aging 26 2005 373 382 (Pubitemid 40082721)
76. S.K. Kaasinen, L. Harvey, A.J. Reynolds, I.A. Hendry Autophagy generates retrogradely transported organelles: A hypothesis Int J Dev Neurosci 26 2008 625 634
77. C.W. Berridge, B.D. Waterhouse The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes Brain Res Brain Res Rev 42 2003 33 84 (Pubitemid 36369264)
78. D.C. German, K.F. Manaye, C.L. White 3rd, D.J. Woodward, D.D. McIntire, W.K. Smith Disease-specific patterns of locus coeruleus cell loss Ann Neurol 32 1992 667 676
79. C.F. Murchison, X.Y. Zhang, W.P. Zhang, M. Ouyang, A. Lee, S.A. Thomas A distinct role for norepinephrine in memory retrieval Cell 117 2004 131 143 (Pubitemid 38469904)
80. C.M. Yates, I.M. Ritchie, J. Simpson, A.F. Maloney, A. Gordon Noradrenaline in Alzheimer-type dementia and Down syndrome Lancet 2 1981 39 40 (Pubitemid 11038693)
81. H. Godridge, G.P. Reynolds, C. Czudek, N.A. Calcutt, M. Benton Alzheimer-like neurotransmitter deficits in adult Down's syndrome brain tissue J Neurol Neurosurg Psychiatry 50 1987 775 778 (Pubitemid 17076293)
82. M. Goldstein, L.S. Freedman, R.P. Ebstein, D.H. Park Studies on dopamine-beta-hydroxylase in mental disorders J Psychiatr Res 11 1974 205 210
83. M. Dierssen, I.F. Vallina, C. Baamonde, S. Garcia-Calatayud, M.A. Lumbreras, J. Florez Alterations of central noradrenergic transmission in Ts65Dn mouse, a model for Down syndrome Brain Res 749 1997 238 244 (Pubitemid 27104205)
84. B. Khakpour-Taleghani, R. Lashgari, F. Motamedi, N. Naghdi Effect of reversible inactivation of locus ceruleus on spatial reference and working memory Neuroscience 158 2009 1284 1291
85. R.M. Deacon, A. Croucher, J.N. Rawlins Hippocampal cytotoxic lesion effects on species-typical behaviours in mice Behav Brain Res 132 2002 203 213 (Pubitemid 34462045)
86. J. Lockrow, H. Boger, G. Gerhardt, G. Aston-Jones, D. Bachman, A.C. Granholm A noradrenergic lesion exacerbates neurodegeneration in a Down syndrome mouse model J Alzheimers Dis 23 2011 471 489
87. D.S. Goldstein, C. Holmes, H. Kaufmann, R. Freeman Clinical pharmacokinetics of the norepinephrine precursor L-threo-DOPS in primary chronic autonomic failure Clin Auton Res 14 2004 363 368 (Pubitemid 40193023)
88. H. Kaufmann, D. Saadia, A. Voustianiouk, D.S. Goldstein, C. Holmes, M.D. Yahr Norepinephrine precursor therapy in neurogenic orthostatic hypotension Circulation 108 2003 724 728 (Pubitemid 36999258)
89. D.S. Goldstein, C. Holmes, L. Sewell, S. Pechnik, I.J. Kopin Effects of carbidopa and entacapone on the metabolic fate of the norepinephrine prodrug L-DOPS J Clin Pharmacol 51 2011 66 74
90. N. Herrmann, K.L. Lanctot, L.R. Khan The role of norepinephrine in the behavioral and psychological symptoms of dementia J Neuropsychiatry Clin Neurosci 16 2004 261 276 (Pubitemid 39244552)
91. M.T. Heneka, F. Nadrigny, T. Regen, A. Martinez-Hernandez, L. Dumitrescu-Ozimek, D. Terwel Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine Proc Natl Acad Sci U S A 107 2010 6058 6063
92. B. Oeseburg, G.J. Dijkstra, J.W. Groothoff, S.A. Reijneveld, D.E. Jansen Prevalence of chronic health conditions in children with intellectual disability: A systematic literature review Intellect Dev Disabil 49 2011 59 85
93. A.D. Randall, J. Witton, C. Booth, A. Hynes-Allen, J.T. Brown The functional neurophysiology of the amyloid precursor protein (APP) processing pathway Neuropharmacology 59 2010 243 267
94. G. Kaplan, J.H. Newcorn Pharmacotherapy for child and adolescent attention-deficit hyperactivity disorder Pediatr Clin North Am 58 2011 99 120 xi