Severe neuronal losses with age in the parietal cortex and ventrobasal thalamus of mice transgenic for the human NF-L neurofilament protein

Journal of Comparative Neurology

Volumn 406, Issue 4, 1999, Pages 433-448

  Ma, Demin ^a   Descarries, Laurent ^a   Micheva, Kristina D ^a   Lepage, Yves ^a   Julien, Jean Pierre ^b   Doucet, Guy ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Cytoskeletal anomaly; Lipofuscin; Neurodegenerative disease; Neuronal death; Unbiased cell counting

Indexed keywords

NEUROFILAMENT PROTEIN;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL LOSS; CELL VIABILITY; CELL VOLUME; CYTOSKELETON; FEMALE; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; THALAMUS;

AGING; ANALYSIS OF VARIANCE; ANIMALS; CELL DEATH; CEREBRAL VENTRICLES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; NEUROFILAMENT PROTEINS; NEURONS; OCCIPITAL LOBE; ORGAN SIZE; PARIETAL LOBE; SPECIES SPECIFICITY; THALAMIC NUCLEI; VISUAL CORTEX;

EID: 0033583561     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990419)406:4<433::AID-CNE2>3.0.CO;2-3     Document Type: Article

References (60)

1. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J. 1996. Human ICE/CED-3 protease nomenclature. Cell 87:171.
2. Amenta F, Bongrani S, Cadel S, Ferrante F, Valsecchi B, Zeng YC. 1994. Influence of treatment with L-deprenyl on the structure of the cerebellar cortex of aged rats. Mech Ageing Dev 75:157-167.
3. Beaudet L, Côté F, Houle D, Julien JP. 1993. Different post-transcriptional controls for the human neurofilament light and heavy genes in transgenic mice. Mol Brain Res 18:23-31.
4. Beaulieu C. 1993. Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 609:284-292.
5. Beaulieu C. 1994. Estimation of the number and size of GABA-containing neurons in the cerebral cortex. Neurosci Protocols 94-080-02-01-20.
6. Cammarata S, Mancardi G, Tabaton M. 1990. Formic acid treatment exposes hidden neurofilament and tau epitopes in abnormal cytoskeletal filaments from patients with progressive supranuclear palsy and Alzheimer's disease. Neurosci Lett 115:351-355.
7. Cataldo AM, Hamilton DJ, Nixon RA. 1994. Lysosomal abnormalities in degenerating neurons link neuronal compromise to senile plaque development in Alzheimer disease. Brain Res 640:68-80.
8. Cataldo AM. Hamilton DJ, Barnett JL, Paskevich PA, Nixon RA. 1996. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci 16:186-199.
9. Collard JF, Côté F, Julien JP. 1995. Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375: 61-64.
10. Côté F, Collard JF, Julien JP. 1993. Progressive neuropathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell 73:35-46.
11. Cullen KM, Halliday GM, Double KL, Brooks WS, Creasey H, Broe GA. 1997. Cell loss in the nucleus basalis is related to regional cortical atrophy in Alzheimer's disease. Neuroscience 78:641-652.
12. Curcio CA, Coleman PD. 1982. Stability of neuron number in cortical barrels of aging mice. J Comp Neurol 212:158-172.
13. Debus E, Weber K, Osborn M. 1983. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25:193-203.
14. Flood DG, Coleman PD. 1988. Neuron numbers and sizes in aging brain: comparisons of human, monkey, and rodent data. Neurobiol Aging 9:453-463.
15. Gai WP, Vickers JC, Blumbergs PC, Blessing WW. 1994. Loss of non-phosphorylated neurofilament immunoreactivity, with preservation of tyrosine hydroxylase, in surviving substantia nigra neurons in Parkinson's disease. J Neurol Neurosurg Psychiatry 57:1039-1046.
16. Goldman JE, Yen SH, Chiu FC, Peress NS. 1983. Lewy bodies of Parkinson's disease contain neurofilament antigens. Science 221:1082-1084.
17. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT. 1997. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 41:17-24.
18. Hamori J, Savy C, Madarasz M, Somogyi J, Takacs J, Verley R, Farkas-Bargeton E. 1986. Morphological alterations in subcortical vibrissal relays following vibrissal follicle destruction at birth in the mouse. J Comp Neurol 254:166-183.
19. Heumann D, Leuba G. 1983. Neuronal death in the development and aging of the cerebral cortex of the mouse. Neuropathol Appl Neurobiol 9:297-311.
20. Hof PR, Morrison JH. 1990. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex. J Comp Neurol 301:55-64.
21. Hof PR, Cox K, Morrison JH. 1990. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex. J Comp Neurol 301:44-54.
22. Julien JP, Tretjakoff I, Beaudet L, Peterson A. 1987. Expression and assembly of a human neurofilament protein in transgenic mice provide a novel neuronal marking system. Genes Dev 1:1085-1095.
23. Julien J-P, Côté F, Collard J-F. 1995. Mice overexpressing the human neurofilament heavy gene as a model of ALS. Neurobiol Aging 16:487-492.
24. Lee MK, Marszalck JR, Cleveland DW. 1994. A mutant neurofilament subunit causes massive, selective motor neuron death: implications for the pathogenesis of human motor neuron disease. Neuron 13:975-988.
25. Leuba G, Heumann D, Rabinowicz T. 1978. Postnatal development of the mouse cerebral neocortex. III. Some dynamical aspects. J Hirnforsch 19:301-312.
26. Ma D, Descarries L, Julien JP, Doucet G. 1995. Abnormal perikaryal accumulation of neurofilament light protein in the cerebral cortex and thalamus of mice transgenic for human NF-L: sequence of postnatal development. Neuroscience 68:135-149.
27. Ma XY, Su YB, Zhang FR, Li JF. 1996. Effects of vitamin E on the blastogenic response of splenocytes and lipofuscin contents in the hearts and brains of aged mice. J Environ Pathol Toxicol Oncol 15:51-53.
28. Manetto V, Sternberger NH, Perry G, Sternberger LA, Gambetti P. 1988. Phosphorylation of neurofilaments is altered in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 47:642-653.
29. Martinou J-C, Sadoul R. 1996. ICE-like proteases execute the neuronal death program. Curr Opin Neurobiol 6:609-614.
30. Mathieu JF, Ma D, Descarries L, Vallée A, Parent A, Julien JP, Doucet G. 1995. CNS distribution and overexpression of neurofilament light proteins (NF-L) in mice transgenic for the human NF-L: aberrant accumulation in thalamic perikarya. Exp Neurol 132:134-146.
31. Micheva KD, Beaulieu C. 1995. Postnatal development of GABA neurons in the rat somatosensory barrel cortex: a quantitative study. Eur J Neurosci 7:419-430.
32. Monji A, Morimoto N, Okuyama I, Yamashita N, Tashiro N. 1994. Effect of dietary vitamin E on lipofuscin accumulation with age in the rat brain. Brain Res 634:62-68.
33. Moore WA, Davey VA, Weindruch R, Walford R, Ivy GO. 1995. The effect of caloric restriction on lipofuscin accumulation in mouse brain with age. Gerontology 41:173-185.
34. Mrini A, Moukhles H, Bosler O, Jacomy H, Doucet G. 1995. Efficient immunodetection of protein antigens in glutaraldehyde-fixed brain tissue. J Histochem Cytochem 43:1285-1291.
35. Munoz DG, Greene C, Perl DP, Selkoe DJ. 1988. Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J Neuropathol Exp Neurol 47:9-18.
36. Nakanishi H, Amano T, Sastradipura DF, Yoshimine Y, Tsukuba T, Tanabe K, Hirotsu I, Ohono T. Yamamoto K. 1997. Increased expression of cathepsins E and D in neurons of the aged rat brain and their colocalization with lipofuscin and carboxy-terminal fragments of Alzheimer amyloid precursor protein. J Neurochem 68:739-749.
37. Nixon RA, Sihag RK. 1991. Neurofilament phosphorylation: a new look at regulation and function. Trends Neurosci 14:501-506.
38. Paxinos G, C Watson. 1986. The rat brain in stereotaxic coordinates. Sydney: Academic Press.
39. Paxinos G, Törk I, Tecott LH, Valentino KL. 1991. Atlas of the developing rat brain. San Diego: Academic Press.
40. Portera-Cailliau C, Hedreen JC, Price DL, Koliatsos VE. 1995. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 15:3775-3787.
41. Portera-Cailliau C, Sung CH, Nathans J, Adler R. 1994. Apoptotic photoreceptor cell death in mouse models of retinitis-pigmentosa. Proc Natl Acad Sci USA 91:974-978.
42. Probst A, Anderton BH, Ulrich J, Kohler R, Kahn J, Heitz PU. 1983. Pick's disease: an immunocytochemical study of neuronal changes monoclonal antibodies show that Pick bodies share antigenic determinants with neurofibrillary tangles and neurofilaments. Acta Neuropathol 60:175-182.
43. Schmidt ML, Murray J, Lee VM, Hill WD, Wertkin A, Trojanowski JQ. 1991. Epitope map of neurofilament protein domains in cortical and peripheral nervous system Lewy bodies. Am J Pathol 139:53-65.
44. Schuz A, Palm G. 1989. Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286:442-455.
45. Schwartz LM, Milligan CE. 1996. Cold thoughts of death: the role of ICE proteases in neuronal cell death. Trends Neurosci 19:555-562.
46. Smale G, Nichols NR, Brady DR, Finch CE, Horton WE. 1995. Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 133:225-230.
47. Su JH, Anderson AJ, Cummings BJ, Cotman CW. 1994. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5:2529-2533.
48. Toyoshima I, Yamamoto A, Masamune O, Satake M. 1989. Phosphorylation of neurofilament proteins and localization of axonal swellings in motor neuron disease. J Neurol Sci 89:269-277.
49. Troost D, Sillevis SP, de Jong JM, Swaab DF. 1992. Neurofilament and glial alterations in the cerebral cortex in amyotrophic lateral sclerosis. Acta Neuropathol 84:664-673.
50. Ulrich J, Anderton BH, Probst A. 1987a. Alzheimer dementia: a study of the senile plaque with antisera and a monoclonal antibody specific for neurofilament proteins. Acta Histochem 34(Suppl):115-121.
51. Ulrich J, Haugh M, Anderton BH, Probst A, Lautenschlager C, His B. 1987b. Alzheimer dementia and Pick's disease: neurofibrillary tangles and Pick bodies are associated with identical phosphorylated neurofilament epitopes. Acta Neuropathol 73:240-246.
52. Vickers JC, Morrison JH, Friedrich VL, Elder GA, Perl DP, Katz RN. Lazzarini RA. 1994. Age-associated and cell-type-specific neurofibrillary pathology in transgenic mice expressing the human midsize neurofilament subunit. J Neurosci 14:5603-5612.
53. von Zglinicki T, Brunk UT. 1993. Intracellular interactions under oxidative stress and aging: a hypothesis. Z Gerontol 26:215-220.
54. Windrem MS, Finlay BL. 1991. Thalamic ablations and neocortical development: alterations of cortical cytoarchitecture and cell number. Cereb Cortex 1:220-240.
55. Xu Z, Cork LC, Griffin JW, Cleveland DW. 1993. Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell 73:23-33.
56. Yin D, 1996. Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic Biol Med 21:871-888
57. Yin D, Yuan X, Brunk UT. 1995. Test-tube simulated lipofuscinogenesis. Effect of oxidative stress on autophagocytotic degradation. Mech Ageing Dev 81:37-50.
58. Zhang H, Sternberger NH, Rubinstein LJ, Herman MM, Binder LI, Sternberger LA. 1989. Abnormal processing of multiple proteins in Alzheimer disease. Proc Natl Acad Sci USA 86:8045-8049.
59. Zilles K. 1985. The cortex of the rat. A stereotaxic atlas. Berlin: Springer-Verlag.
60. Zilles K, Wree A. 1995. Cortex: areal and laminar structure. In: Paxinos M, editor. The rat nervous system, 2nd Ed. San Diego: Academic Press, p 649-685.