Differential expression of interneuron populations and correlation with amyloid-β deposition in the olfactory cortex of an aβPP/PS1 transgenic mouse model of alzheimer's disease

Journal of Alzheimer's Disease

Volumn 31, Issue 1, 2012, Pages 113-129

  Saiz Sanchez, Daniel ^a   Ubeda Baon, Isabel ^a   De La Rosa Prieto, Carlos ^a   Martinez Marcos, Alino ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

Alzheimer's disease; amyloid; calcium binding protein; entorhinal cortex; interneuron; piriform cortex; somatostatin; transgenic

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CALBINDIN; CALRETININ; PARVALBUMIN; PRESENILIN 1; SOMATOSTATIN;

AGE; ALZHEIMER DISEASE; AMYLOID NEUROPATHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENTORHINAL CORTEX; FEMALE; INTERNEURON; MOUSE; NONHUMAN; OLFACTORY CORTEX; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TRANSGENIC MOUSE;

EID: 84863978711     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-111889     Document Type: Article

References (63)

1. Fotuhi M, Hachinski V, Whitehouse PJ (2009) Changing perspectives regarding late-life dementia. Nat Rev Neurol 5, 649-658.
2. Perrin RJ, Fagan AM, Holtzman DM (2009) Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461, 916-922.
3. Hernandez F, Avila J (2008) Tau aggregates and tau pathology. J Alzheimers Dis 14, 449-452.
4. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81, 741-766. (Pubitemid 32267077)
5. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
6. Price JL, Morris JC (2004) Sowhatiftangles precede plaques? Neurobiol Aging 25, 721-723; discussion 743-726.
7. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185.
8. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259.
9. Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neurobiol Aging 12, 295-312.
10. Hawkes CH, Doty RL (2009) The Neurology of Olfaction, Cambridge University Press, Cambridge, pp. 153-214.
11. Djordjevic J, Jones-Gotman M, De Sousa K, Chertkow H (2008) Olfaction in patients with mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 29, 693-706. (Pubitemid 351410525)
12. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14, 1-19.
13. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneuronsofthe neocortical inhibitory system. Nat Rev Neurosci 5, 793-807.
14. Kawaguchi Y, Kondo S (2002) Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31, 277-287. (Pubitemid 36877376)
15. Matyas F, Freund TF, Gulyas AI (2004) Immunocytochemi-cally defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus 14, 460-481. (Pubitemid 38868046)
16. Geula C, Bu J, Nagykery N, Scinto LF, Chan J, Joseph J, Parker R, Wu CK (2003) Loss of calbindin-D28k from aging human cholinergic basal forebrain: Relation to neuronal loss. J Comp Neurol 455, 249-259.
17. Saiz-Sanchez D, Ubeda-Banon I, de la Rosa-Prieto C, Argandona-Palacios L, Garcia-Munozguren S, Insausti R, Martinez-Marcos A (2010) Somatostatin, tau, and beta-amyloid within the anterior olfactory nucleus in Alzheimer disease. Exp Neurol 223, 347-350.
18. Solodkin A, Veldhuizen SD, Van Hoesen GW (1996) Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer's disease. J Neurosci 16, 3311-3321. (Pubitemid 26142364)
19. Koliatsos VE, Kecojevic A, Troncoso JC, Gastard MC, Bennett DA, Schneider JA (2006) Early involvement of small inhibitory cortical interneurons in Alzheimer's disease. Acta Neuropathol 112,147-162.
20. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci USA 100, 9572-9577. (Pubitemid 37033969)
21. Doty RL (2003) Handbook of olfaction and gustation. Informa Healthcare, pp. 139-201.
22. Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R (1999) Subfield-and layer-specific changes in parvalbu-min, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer's disease. Neuroscience 92, 515-532. (Pubitemid 29268040)
23. Epelbaum J, Guillou JL, Gastambide F, Hoyer D, Duron E, Viollet C (2009) Somatostatin, Alzheimer's disease and cognition: An old story coming of age? Prog Neurobiol 89, 153-161.
24. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damageinthe ageing human brain. Nature 429, 883-891. (Pubitemid 38843301)
25. Davies P, Katzman R, Terry RD (1980) Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 288, 279-280. (Pubitemid 11165878)
26. Davies P, Terry RD (1981) Cortical somatostatin-like immunoreactivity in cases of Alzheimer's disease and senile dementia of the Alzheimer type. Neurobiol Aging 2, 9-14. (Pubitemid 11082130)
27. Hama E, Saido TC (2005) Etiology of sporadic Alzheimer's disease: Somatostatin, neprilysin, and amyloid beta peptide. Med Hypotheses 65, 498-500. (Pubitemid 40956947)
28. Mattson MP (1994) Calcium and neuronal injury in Alzheimer's disease. Contributions of beta-amyloid precursor protein mismetabolism, free radicals, and metabolic compromise. Ann N Y Acad Sci 747, 50-76.
29. Guo Q, Sopher BL, Furukawa K, Pham DG, Robinson N, Martin GM, Mattson MP (1997) Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: Involvement of calcium and oxyradicals. J Neurosci 17, 4212-4222. (Pubitemid 27220612)
30. Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6, 337-350.
31. Foster TC (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6, 319-325. (Pubitemid 46785137)
32. Hof PR, Nimchinsky EA, Celio MR, Bouras C, Morrison JH (1993) Calretinin-immunoreactive neocortical interneu-rons are unaffected in Alzheimer's disease. Neurosci Lett 152, 145-148.
33. Attems J, Preusser M, Grosinger-Quass M, Wagner L, Lintner F, Jellinger K (2008) Calcium-binding protein secretagogin-expressing neurones in the human hippocampus are largely resistant to neurodegeneration in Alzheimer's disease. Neu-ropathol Appl Neurobiol 34, 23-32.
34. Brady DR, Mufson EJ (1997) Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain. Neuroscience 80, 1113-1125. (Pubitemid 27359796)
35. Sampson VL, Morrison JH, Vickers JC (1997) The cellular basis for the relative resistance of parvalbumin and calre-tinin immunoreactive neocortical neurons to the pathology of Alzheimer's disease. Exp Neurol 145, 295-302. (Pubitemid 27244303)
36. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: Evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13, 159-170. (Pubitemid 38111354)
37. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, Frosch MP (2006) Characterization ofamyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24, 516-524. (Pubitemid 44716680)
38. Wang J, Tanila H, Puolivali J, Kadish I, van Groen T (2003) Gender differences in the amount and deposition of amyloid-beta in APPswe and PS1 double transgenic mice. Neurobiol Dis 14, 318-327. (Pubitemid 37543511)
39. Guillery RW (2002) On counting and counting errors. J Comp Neurol 447, 1-7. (Pubitemid 34298840)
40. Adalbert R, Nogradi A, Babetto E, Janeckova L, Walker SA, Kerschensteiner M, Misgeld T, Coleman MP (2009) Severely dystrophic axons at amyloid plaques remain continuous and connected to viable cell bodies. Brain 132, 402-416.
41. Wesson DW, Levy E, Nixon RA, Wilson DA (2010) Olfactory dysfunction correlates with amyloid-beta burden in an Alzheimer's disease mouse model. J Neurosci 30, 505-514.
42. Young JW, Sharkey J, Finlayson K (2009) Progressive impairment in olfactory working memory in a mouse model of mild cognitive impairment. Neurobiol Aging 30, 1430-1443.
43. Lemmens MA, Sierksma AS, Rutten BP, Dennissen F, Stein-busch HW, Lucassen PJ, Schmitz C (2011) Age-related changesofneuron numbersinthefrontal cortexofatransgenic mouse model of Alzheimer's disease. Brain Struct Funct 216, 227-237.
44. Popovic M, Caballero-Bleda M, Kadish I, Van Groen T (2008) Subfield and layer-specific depletion in calbindin-D28K, calretinin and parvalbumin immunoreactivity in the dentate gyrus of amyloid precursor protein/presenilin 1 trans-genic mice. Neuroscience 155, 182-191.
45. Takahashi H, Brasnjevic I, Rutten BP, Van Der Kolk N, Perl DP, Bouras C, Steinbusch HW, Schmitz C, Hof PR, Dickstein DL (2010) Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer's disease. Brain Struct Funct 214, 145-160.
46. Poo C, Isaacson JS (2009) Odor representations in olfactory cortex: "Sparse" coding, global inhibition, and oscillations. Neuron 62, 850-861.
47. Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216.
48. Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T, Dokka K, Baldwin KK (2011) Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220.
49. Lazarov O, Peterson LD, Peterson DA, Sisodia SS (2006) Expression of a familial Alzheimer's disease-linked presenilin-1 variant enhances perforant pathway lesion-induced neuronal loss in the entorhinal cortex. J Neurosci 26, 429-434. (Pubitemid 43237106)
50. Supnet C, Bezprozvanny I (2010) The dysregulation of intra-cellular calcium in Alzheimer disease. Cell Calcium 47, 183-189.
51. Ramos B, Baglietto-Vargas D, del Rio JC, Moreno-Gonzalez I, Santa-Maria C, Jimenez S, Caballero C, Lopez-Tellez JF, Khan ZU, Ruano D, Gutierrez A, Vitorica J (2006) Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease. Neurobiol Aging 27, 1658-1672. (Pubitemid 44363105)
52. Baglietto-Vargas D, Moreno-Gonzalez I, Sanchez-Varo R, Jimenez S, Trujillo-Estrada L, Sanchez-Mejias E, Torres M, Romero-Acebal M, Ruano D, Vizuete M, Vitorica J, Gutierrez A (2010) Calretinin interneurons are early targets of extracellular amyloid-beta pathology in PS1/AbetaPP Alzheimer mice hippocampus. J Alzheimers Dis 21, 119-132.
53. Moreno-Gonzalez I, Baglietto-Vargas D, Sanchez-Varo R, Jimenez S, Trujillo-Estrada L, Sanchez-Mejias E, Del Rio JC, Torres M, Romero-Acebal M, Ruano D, Vizuete M, Vitorica J, Gutierrez A (2009) Extracellular amyloid-beta and cytotoxic glial activation induce significant entorhinal neuron loss in young PS1 (M146L)/APP (751SL) mice. J Alzheimers Dis 18, 755-776.
54. Morrison JH, Rogers J, Scherr S, Benoit R, Bloom FE (1985) Somatostatin immunoreactivity in neuritic plaques of Alzheimer's patients. Nature 314, 90-92. (Pubitemid 15142024)
55. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sak-mannB (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1, 279-285. (Pubitemid 128712317)
56. Saito T, Iwata N, Tsubuki S, Takaki Y, Takano J, Huang SM, Suemoto T, Higuchi M, Saido TC (2005) Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation. Nat Med 11, 434-439. (Pubitemid 40562335)
57. van de Nes JA, Sandmann-Keil D, Braak H (2002) Interstitial cells subjacent to the entorhinal region expressing somatostatin-28 immunoreactivity are susceptible to development of Alzheimer's disease-related cytoskeletal changes. Acta Neuropathol 104, 351-356. (Pubitemid 36075398)
58. Tamminga CA, Foster NL, Fedio P, Bird ED, Chase TN (1987) Alzheimer's disease: Low cerebral somatostatin levels correlate with impaired cognitive function and cortical metabolism. Neurology 37, 161-165.
59. Craft S, Asthana S, Newcomer JW, Wilkinson CW, Matos IT, Baker LD, Cherrier M, Lofgreen C, Latendresse S, Petrova A, Plymate S, Raskind M, Grimwood K, Veith RC (1999) Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Arch Gen Psychiatry 56, 1135-1140.
60. Citron M, Westaway D, Xia W, Carlson G, Diehl T, Levesque G, Johnson-Wood K, Lee M, Seubert P, Davis A, Kholodenko D, Motter R, Sherrington R, Perry B, Yao H, Strome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St George Hyslop P, Selkoe DJ (1997) Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat Med 3, 67-72. (Pubitemid 27019143)
61. Chetelat G, Villemagne VL, Pike KE, Ellis KA, Bourgeat P, Jones G, O'Keefe GJ, Salvado O, Szoeke C, Martins RN, Ames D, Masters CL, Rowe CC (2011) Independent contribution of temporal beta-amyloid deposition to memory decline in the pre-dementia phase of Alzheimer's disease. Brain 134, 798-807.
62. Buxbaum JD, Thinakaran G, Koliatsos V, O'Callahan J, Slunt HH, Price DL, Sisodia SS (1998) Alzheimer amyloid protein precursor in the rat hippocampus: Transport and processing through the perforant path. J Neurosci 18, 9629-9637. (Pubitemid 28543744)
63. Sheng JG, Price DL, Koliatsos VE (2002) Disruption of corticocortical connections ameliorates amyloidburdeninter-minal fields in a transgenic model of Abeta amyloidosis. J Neurosci 22, 9794-9799. (Pubitemid 35332863)