Early behavioral changes and quantitative analysis of neuropathological features in murine prion disease: Stereological analysis in the albino Swiss mice model

Prion

Volumn 5, Issue 3, 2011, Pages 215-227

  Borner, Roseane ^a   Bento Torres, João ^a   Souza, Diego R V ^a   Sadala, Danyelle B ^a   Trevia, Nonata ^a   Farias, José Augusto ^a   Lins, Nara ^a   Passos, Aline ^a   Quintairos, Amanda ^a   Diniz, José Antônio ^b   Perry, Victor Hugh ^c   Vasconcelos, Pedro Fernando ^b   Cunningham, Colm ^d   Picanço Diniz, Cristovam Wanderley ^a  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b INSTITUTO EVANDRO CHAGAS   (Brazil)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Albino Swiss mice; Behavioral changes; Neuropathology; Optical fractionator; Prion disease

Indexed keywords

AMINE; DEXTRAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BEHAVIOR CHANGE; BIOTINYLATION; BRAIN HOMOGENATE; CLUSTER ANALYSIS; CONTROLLED STUDY; DENTATE GYRUS; DISCRIMINANT ANALYSIS; DISEASE COURSE; EXTRACELLULAR MATRIX; FEMALE; HIPPOCAMPAL CA1 REGION; MICROGLIA; MOSSY FIBER; MOUSE; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PRION DISEASE; QUANTITATIVE ANALYSIS; STATISTICAL ANALYSIS; STEREOMETRY;

MURINAE; MUS;

EID: 80052807751     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.5.3.16936     Document Type: Article

References (69)

1. Prusiner SB. Shattuck lecture - neurodegenerative diseases and prions. N Engl J Med 2001; 344:1516-26.
2. Aguzzi A, Sigurdson C, Heikenwaelder M. Molecular mechanisms of prion pathogenesis. Annu Rev Pathol 2008; 3:11-40.
3. Chiti Z, Knutsen OM, Betmouni S, Greene JR. An integrated, temporal study of the behavioral, electrophysiological and neuropathological consequences of murine prion disease. Neurobiology of disease 2006; 22:363-73.
4. Cunningham CR, Deacon H, Wells D, Boche S. Waters CP. Diniz, et al. Synaptic changes characterize early behavioral changes in the ME7 model of murine prion disease. Eur J Neurosci 2003; 17:2147-55.
5. Betmouni S, Perry VH. The acute inflammatory response in CNS following injection of prion brain homogenate or normal brain homogenate. Neuropathol Appl Neurobiol 1999; 25:20-8.
6. Betmouni S, Perry VH, Gordon JL. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 1996; 74:1-5.
7. Gray BC, Siskova Z, Perry VH, O'Connor V. Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology. Neurobiology of disease 2009; 35:63-74.
8. Franklin S, Love S, Greene J, Betmouni S. Loss of Perineuronal Net in ME7 Prion Disease. J Neuropathol Exp Neurol 2008; 67:189-99.
9. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991; 231:482-97.
10. Schmitz C, Hof PR. Design-based stereology in neuroscience. Neuroscience 2005; 130:813-31.
11. Stark AK, Pelvig DP, Jorgensen AM, Andersen BB, Pakkenberg B. Measuring morphological and cellular changes in Alzheimer's dementia: a review emphasizing stereology. Current Alzheimer research 2005; 2:449-81.
12. West MJ. Design-based stereological methods for counting neurons. Prog Brain Res 2002; 135:43-51.
13. Bonthius DJ, McKim R, Koele L, Harb H, Karacay B, Mahoney J, et al. Use of frozen sections to determine neuronal number in the murine hippocampus and neocortex using the optical disector and optical fractionator. Brain Res Brain Res Protoc 2004; 14:45-57.
14. Gundersen H, Jensen E. The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987; 147:229-63.
15. Casarrubea M, Sorbera F, Crescimanno G. Multivariate analysis of the modifications induced by an environmental acoustic cue on rat exploratory behavior. Physiol Behav 2008; 93:687-96.
16. Casarrubea M, Sorbera F, Crescimanno G. Multivariate data handling in the study of rat behavior: an integrated approach. Behav Res Methods 2009; 41:772-81.
17. Hilborn JV, Strauss E, Hultsch DF, Hunter MA. Intraindividual variability across cognitive domains: investigation of dispersion levels and performance profiles in older adults. J Clin Exp Neuropsychol 2009; 31:412-24.
18. Bitsika V, Sharpley CF, Orapeleng S. An exploratory analysis of the use of cognitive, adaptive and behavioral indices for cluster analysis of ASD subgroups. J Intellect Disabil Res 2008; 52:973-85.
19. Hybels CF, Blazer DG, Pieper CF, Landerman LR, Steffens DC. Profiles of depressive symptoms in older adults diagnosed with major depression: latent cluster analysis. Am J Geriatr Psychiatry 2009; 17:387-96.
20. Lane AE, Young RL, Baker AE, Angley MT. Sensory Processing Subtypes in Autism: Association with Adaptive Behavior. J Autism Dev Disord 2009.
21. Cancellotti E, Barron RM, Bishop MT, Hart P, Wiseman F, Manson JC. The role of host PrP in Transmissible Spongiform Encephalopathies. Biochim Biophys Acta 2007; 1772:673-80.
22. Moody LR, Herbst AJ, Aiken JM. Upregulation of interferon-gamma-induced genes during prion infection. J Toxicol Environ Health A 2011; 74:146-53.
23. Perry VH. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun 2004; 18:407-13.
24. Kranich J, Krautler NJ, Falsig J, Ballmer B, Li S, Hutter G, et al. Engulfment of cerebral apoptotic bodies controls the course of prion disease in a mouse strain-dependent manner. J Exp Med 2010; 207:2271-81.
25. Lloyd SE, Onwuazor ON, Beck JA, Mallinson G, Farrall M, Targonski P, et al. Identification of multiple quantitative trait loci linked to prion disease incubation period in mice. Proc Natl Acad Sci USA 2001; 98:6279-83.
26. Sandberg MK, Al-Doujaily H, Sharps B, Clarke AR, Collinge J. Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 2011; 470:540-2.
27. Iyegbe CO, Abiola OO, Towlson C, Powell JF, Whatley SA. Evidence for varied aetiologies regulating the transmission of prion disease: implications for understanding the heritable basis of prion incubation times. PLoS One 2010; 5:14186.
28. Foster JD, Davies DJ, Fraser H. Primary retinopathy in scrapie in mice deprived of light. Neurosci Lett 1986; 72:111-4.
29. Cunningham C. Mouse behavioral studies and what they can teach us about prion diseses. In: Brown D, Ed. Neurodegeneration and prion disese. New York, NY: Springer Science + Business Media, Inc. 2005; 111-37.
30. Paxinos G, Franklin K. The mouse brain in stereotaxic coordinates. London, UK: Academic Press 2001.
31. Deacon R, Raley J, Perry V, Rawlins J. Burrowing into prion diasease. Neuroreport 2001; 12:2053-7.
32. Streit WJ. Microglial response to brain injury: a brief synopsis. Toxicol Pathol 2000; 28:28-30.
33. Bruckner G, Grosche J, Hartlage-Rubsamen M, Schmidt S, Schachner M. Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 2003; 26:37-50.
34. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature 2000; 405:951-5.
35. Edgar MA, Rosenblum MK. The differential diagnosis of central nervous system tumors: a critical examination of some recent immunohistochemical applications. Archives of pathology & laboratory medicine 2008; 132:500-9.
36. Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, et al. Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 2004; 1017:21-31.
37. Kumar SS, Buckmaster PS. Neuron-specific nuclear antigen NeuN is not detectable in gerbil subtantia nigra pars reticulata. Brain Res 2007; 1142:54-60.
38. Darlington PJ, Goldman JS, Cui QL, Antel JP, Kennedy TE. Widespread immunoreactivity for neuronal nuclei in cultured human and rodent astrocytes. Journal of neurochemistry 2008; 104:1201-9.
39. Zhao N, Zhong C, Wang Y, Zhao Y, Gong N, Zhou G, et al. Impaired hippocampal neurogenesis is involved in cognitive dysfunction induced by thiamine deficiency at early pre-pathological lesion stage. Neurobiology of disease 2008; 29:176-85.
40. von Bohlen Und Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell and tissue research 2007; 329:409-20.
41. Takahashi T, Zhu Y, Hata T, Shimizu-Okabe C, Suzuki K, Nakahara D. Intracranial self-stimulation enhances neurogenesis in hippocampus of adult mice and rats. Neuroscience 2008.
42. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development (Cambridge, England) 2003; 130:391-9.
43. Clark PJ, Brzezinska WJ, Thomas MW, Ryzhenko NA, Toshkov SA, Rhodes JS. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 2008; 155:1048-58.
44. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, et al. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Molecular and cellular neurosciences 2003; 24:603-13.
45. Slomianka L, West M. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 2005; 136:757-67.
46. Glaser EM, Wilson PD. The coefficient of error of optical fractionator population size estimates: a computer simulation comparing three estimators. Journal of Microscopy 1998; 192:163-71.
47. Ayres M, Ayres JR M, Ayres DL, SANTOS AS. BioEstat 4.0: Aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém: Sociedade Civil Mamirauá, Brasília CNPq 2005.
48. Amaral DG, Scharfman HE, Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 2007; 163:3-22.
49. Guenther K, Deacon RM, Perry VH, Rawlins JN. Early behavioral changes in scrapie-affected mice and the influence of dapsone. Eur J Neurosci 2001; 14:401-9.
50. Betmouni S, Deacon RMJ, Rawlins JNP, Perry VH. Behavioral consequences of prion disease targeted to the hippocampus in a mouse model of scrapie. Psychobiology 1999; 27:63-71.
51. Cunningham C, Wilcockson D, Campion S, Lunnon K, Perry V. Central and Systemic Endotoxin Challenges Exacerbate the Local Inflammatory Response and Increase Neuronal Death during Chronic Neurodegeneration. The Journal of Neuroscience 2005; 25:9275-84.
52. Moreau PH, Cosquer B, Jeltsch H, Cassel JC, Mathis C. Neuroanatomical and behavioral effects of a novel version of the cholinergic immunotoxin mu p75-saporin in mice. Hippocampus 2008; 18:610-22.
53. Kobayashi K. Targeting the hippocampal mossy fiber synapse for the treatment of psychiatric disorders. Mol Neurobiol 2009; 39:24-36.
54. Broom KA, Anthony DC, Lowe JP, Griffin JL, Scott H, Blamire AM, et al. MRI and MRS alterations in the preclinical phase of murine prion disease: association with neuropathological and behavioral changes. Neurobiology of disease 2007; 26:707-17.
55. Deacon RM, Rawlins JN. Hippocampal lesions, species-typical behaviours and anxiety in mice. Behav Brain Res 2005; 156:241-9.
56. Guentchev M, Groschup MH, Kordek R, Liberski PP, Budka H. Severe, early and selective loss of a subpopulation of GABAergic inhibitory neurons in experimental transmissible spongiform encephalopathies. Brain Pathol 1998; 8:615-23.
57. Ermolayev V, Cathomen T, Merk J, Friedrich M, Hartig W, Harms GS, et al. Impaired axonal transport in motor neurons correlates with clinical prion disease. PLoS Pathog 2009; 5:1000558.
58. Picanco-Diniz CW, Boche D, Gomes-Leal W, Perry VH, Cunningham C. Neuropil and neuronal changes in hippocampal NADPH-diaphorase histochemistry in the ME7 model of murine prion disease. Neuropathol Appl Neurobiol 2004; 30:292-303.
59. Toyoshima I, Sugawara M, Kato K, Wada C, Hirota K, Hasegawa K, et al. Kinesin and cytoplasmic dynein in spinal spheroids with motor neuron disease. J Neurol Sci 1998; 159:38-44.
60. Cunningham C, Deacon RM, Chan K, Boche D, Rawlins JN, Perry VH. Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits. Neurobiology of disease 2005; 18:258-69.
61. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, et al. The most infectious prion protein particles. Nature 2005; 437:257-61.
62. Aguzzi A, O'Connor T. Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat Rev Drug Discov 2010; 9:237-48.
63. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, et al. Abeta oligomer-induced aberrations in synapse composition, shape and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007; 27:796-807.
64. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathol 2009; 118:167-79.
65. Nimmrich V, Ebert U. Is Alzheimer's disease a result of presynaptic failure? Synaptic dysfunctions induced by oligomeric beta-amyloid. Rev Neurosci 2009; 20:1-12.
66. Chen TJ, Wang DC, Chen SS. Amyloid-beta interrupts the PI3K-Akt-mTOR signaling pathway that could be involved in brain-derived neurotrophic factor-induced Arc expression in rat cortical neurons. Journal of neuroscience research 2009; 87:2297-307.
67. Westaway D, Goodman PA, Mirenda CA, McKinley MP, Carlson GA, Prusiner SB. Distinct prion proteins in short and long scrapie incubation period mice. Cell 1987; 51:651-62.
68. Lloyd S, Mead S, Collinge J. Genetics of Prion Disease. Top Curr Chem 2011.
69. Felton LM, Cunningham C, Rankine EL, Waters S, Boche D, Perry VH. MCP-1 and murine prion disease: separation of early behavioral dysfunction from overt clinical disease. Neurobiology of disease 2005; 20:283-95.