Late onset neurodegeneration in the Cln3 -/- mouse model of juvenile neuronal ceroid lipofuscinosis is preceded by low level glial activation

Brain Research

Volumn 1023, Issue 2, 2004, Pages 231-242

  Pontikis, Charlie C ^a,b,c   Cella, Claire V ^a,b   Parihar, Nisha ^a,b   Lim, Ming J ^a,c   Chakrabarti, Shubhodeep ^a,b   Mitchison, Hannah M ^d   Mobley, William C ^e   Rezaie, Payam ^b,f   Pearce, David A ^g   Cooper, Jonathan D ^a,b,c,e  

^a Pediat Storage Disorders Laboratory   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c 4th Fl Rayne Bldg 5 Univ S ^*  (United Kingdom)

^d ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f OPEN UNIVERSITY   (United Kingdom)

^g UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Astrocytosis; CLN3; GABAergic interneuron; JNCL; Microglial activation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ATROPHY; CONTROLLED STUDY; FEMALE; GLIA CELL; GLIOSIS; HIPPOCAMPUS; MALE; MICROGLIA; MORPHOLOGY; MOUSE; MOUSE STRAIN; NEOCORTEX; NERVE DEGENERATION; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PATHOLOGY; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; UPREGULATION;

AGE FACTORS; ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ASTROCYTES; BRAIN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL COUNT; CELL SIZE; CELL SURVIVAL; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MOLECULAR CHAPERONES; NERVE DEGENERATION; NEUROGLIA; NEURONAL CEROID-LIPOFUSCINOSES; PARVALBUMINS; SOMATOSTATIN; STAINING AND LABELING; STATISTICS, NONPARAMETRIC;

EID: 4544285361     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.07.030     Document Type: Article

References (43)

1. M. Abercrombie Estimation of nuclear populations from microtome sections Anat. Rec. 94 1946 239 247
2. E. Bible, P. Gupta, S.L. Hofmann, and J.D. Cooper Regional and cellular neuropathology in the palmitoyl protein thioesterase-1 (PPT1) null mutant mouse model of infantile neuronal ceroid lipofuscinosis Neurobiol. Dis. 16 2004 346 359
3. H. Braak, and H.H. Goebel Loss of pigment-laden stellate cells: a severe alteration of the isocortex in juvenile neuronal ceroid-lipofuscinosis Acta Neuropathol. (Berl) 42 1978 53 57
4. H. Braak, and H.H. Goebel Pigmentoarchitectonic pathology of the isocortex in juvenile neuronal ceroid-lipofuscinosis: axonal enlargements in layer IIIab and cell loss in layer V Acta Neuropathol. (Berl) 46 1979 79 83
5. H. Braak, E. Braak, F. Gullotta, and H.H. Goebel Pigment-filled appendages of the small spiny neurons: a severe pathological change of the striatum in neuronal ceroid lipofuscinosis Neuropathol. Appl. Neurobiol. 5 1979 389 394
6. A.I. Brooks, S. Chattopadhyay, H.M. Mitchison, R.L. Nussbaum, and D.A. Pearce Functional categorization of gene expression changes in the cerebellum of a Cln3-knockout mouse model for Batten disease Mol. Genet. Metab. 78 2003 17 30
7. S. Chattopadhyay, M. Ito, J.D. Cooper, A.I. Brooks, T.M. Curran, J.M. Powers, and D.A. Pearce DA An autoantibody inhibitory to glutamic acid decarboxylase in the neurodegenerative disorder Batten disease Hum. Mol. Genet. 11 2002 1421 1431
8. S. Chattopadhyay, E. Kriscenski-Perry, D.A. Wenger, and D.A. Pearce An autoantibody to GAD65 in sera of patients with juvenile neuronal ceroid lipofuscinoses Neurology 59 2002 1816 1817
9. J.D. Cooper Progress towards understanding the neurobiology of Batten disease or neuronal ceroid lipofuscinosis Curr. Opin. Neurol. 16 2003 121 128
10. J.D. Cooper, A. Messer, A.K. Feng, J. Chua-Couzens, and W.C. Mobley Apparent loss and hypertrophy of interneurons in a mouse model of neuronal ceroid lipofuscinosis: evidence for partial response to insulin-like growth factor-1 treatment J. Neurosci. 19 1999 2556 2567
11. Î"ex7/8 knock-in mice with the common JNCL mutation exhibit progressive neurologic disease that begins before birth Hum. Mol. Genet. 11 2002 2709 2721
12. C. D'Orlando, M.R. Celio, and B. Schwaller Calretinin and calbindin D-28k, but not parvalbumin protect against glutamate-induced delayed excitotoxicity in transfected N18-RE 105 neuroblastoma-retina hybrid cells Brain Res. 94 2002 181 190
13. T.F. Freund, and G. Buzsáki Interneurons of the hippocampus Hippocampus 6 1996 347 470
14. R.M. Gardiner Clinical features and molecular genetic basis of the neuronal ceroid lipofuscinoses Adv. Neurol. 89 2002 211 215
15. J. Gehrmann, Y. Matsumoto, and G.W. Kreutzberg Microglia: intrinsic immuneffector cell of the brain Brain Res. Brain Res. Rev. 20 1995 269 287
16. H.J. Gundersen, and E.B. Jensen The efficiency of systematic sampling in stereology and its prediction J. Microsc. 147 1987 229 263
17. P. Gupta, A.A. Soyombo, A. Atashband, K.E. Wisniewski, J.M. Shelton, J.A. Richardson, R.E. Hammer, and S.L. Hofmann Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice Proc. Natl. Acad. Sci. U. S. A. 98 2001 13566 13571
18. M. Haltia, J. Rapola, and P. Santavuori Infantile type of so-called neuronal ceroid-lipofuscinosis. Histological and electron microscopic studies Acta Neuropathol. (Berl) 26 1973 157 170
19. M. Haltia, J. Rapola, P. Santavuori, and A. Keranen Infantile type of so-called neuronal ceroid-lipofuscinosis: 2. Morphological and biochemical studies J. Neurol. Sci. 18 1973 269 285
20. R. Herva, J. Tyynelä, A. Hirvasniemi, M. Syrjakallio-Ylitalo, and M. Haltia Northern epilepsy: a novel form of neuronal ceroid-lipofuscinosis Brain Pathol. 10 2000 215 222
21. S.L. Hofmann, and L. Peltonen The neuronal ceroid lipofuscinosis C.R. Scriver A.L. Beaudet W.S. Sly D. Valle 8th ed. The Metabolic and Molecular Basis of Inherited Disease vol III 2001 McGraw-Hill Companies Montreal 3877 3894
22. M. Jeyakumar, R. Thomas, E. Elliot-Smith, D.A. Smith, A.C. van der Spoel, A. d'Azzo, V.H. Perry, T.D. Butters, R.A. Dwek, and F.M. Platt Central nervous system inflammation is a hallmark of pathogenesis in mouse models of GM1 and GM2 gangliosidosis Brain 126 2003 974 987
23. M.L. Katz, H. Shibuya, P.C. Liu, S. Kaur, C.L. Gao, and G.S. Johnson A mouse gene knockout model for juvenile ceroid-lipofuscinosis (Batten disease) J. Neurosci. Res. 57 1999 551 556
24. G.W. Kreutzberg Microglia: a sensor for pathological events in the CNS Trends Neurosci. 19 1996 312 318
25. H.H.D. Lam, H.M. Mitchison, N.D.E. Greene, R.L. Nussbaum, W.C. Mobley, and J.D. Cooper Pathologic involvement of interneurons in mouse models of neuronal ceroid lipofuscinosis Abstr.-Soc. Neurosci. 25 1999 1593
26. H.M. Mitchison, D.J. Bernard, N.D.E. Greene, J.D. Cooper, M.A. Junaid, R.K. Pullarkat, N. Vos, M.H. Breuning, J.W. Owens, W.C. Mobley, R.M. Gardiner, B.D. Lake, P.E.M. Taschner, and R.L. Nussbaum Targeted Disruption of the Cln3 gene provides a mouse model for Batten Disease. The Batten Mouse Model Consortium Neurobiol. Dis. 6 1999 321 334
27. H.M. Mitchison, M.J. Lim, and J.D. Cooper Selectivity and types of cell death in the neuronal ceroid lipofuscinoses (NCLs) Brain Pathol. 14 2004 86 96
28. K. Ohmi, D.S. Greenberg, K.S. Rajavel, S. Ryazantsev, H.H. Li, and E.F. Neufeld Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB Proc. Natl. Acad. Sci. U. S. A. 100 2003 1902 1907
29. M.J. Oswald, G.W. Kay, and D.N. Palmer Changes in GABAergic neuron distribution in situ and in neuron cultures in ovine (OCL6) Batten disease Eur. J. Paediatr. Neurol. 5 Suppl. A 2001 135 142
30. G. Paxinos, and K.B.J. Franklin The Mouse Brain in Stereotaxic Coordinates 2nd edition 2001 Academic Press San Diego
31. G. Raivich, M. Bohatschek, C.U. Kloss, A. Werner, L.L. Jones, and G.W. Kreutzberg Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function Brain Res. Brain Res. Rev. 30 1999 77 105
32. W.J. Streit The role of microglia in regeneration Eur. Arch. Otorhinolaryngol. 1994 S69 S70
33. W.J. Streit Microglial response to brain injury: a brief synopsis Toxicol. Pathol. 28 2000 28 30
34. W.J. Streit Microglia as neuroprotective, immunocompetent cells of the CNS Glia 40 2002 133 139
35. The International Batten Disease Consortium Isolation of a novel gene underlying Batten disease, CLN3 Cell 82 1995 949 957
36. J. Tyynelä, J. Suopanki, P. Santavuori, M. Baumann, and M. Haltia Variant late infantile neuronal ceroid-lipofuscinosis: pathology and biochemistry J. Neuropathol. Exp. Neurol. 56 1997 369 375
37. J. Tyynelä, J.D. Cooper, M.N. Khan, S.J.A. Shemilt, and M. Haltia Specific patterns of storage deposition, neurodegeneration, and glial activation in the hippocampus of patients with neuronal ceroid-lipofuscinoses Brain Pathol. 14 2004 in press
38. U. von Eitzen, R. Egensperger, S. Kosel, E.M. Grasbon-Frodl, Y. Imai, K. Bise, S. Kohsaka, P. Mehraein, and M.B. Graeber Microglia and the development of spongiform change in Creutzfeldt-Jakob disease J. Neuropathol. Exp. Neurol. 57 1998 246 256
39. R. Wada, C.J. Tifft, and R.L. Proia Microglial activation precedes acute neurodegeneration in Sandhoff disease and is suppressed by bone marrow transplantation Proc. Natl. Acad. Sci. U. S. A. 97 2000 10954 10959
40. D. Wahlsten Deficiency of corpus callosum varies with strain and supplier of the mice Brain Res. 239 1982 329 347
41. S.U. Walkley, P.A. March, C.E. Schroeder, S. Wurzelmann, and R.D. Jolly Pathogenesis of brain dysfunction in Batten disease Am. J. Med. Genet. 57 1995 196 203
42. M.J. West, L. Slomianka, and H.J. Gundersen Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator Anat. Rec. 231 1991 482 497
43. D.P. Wolfer, W.E. Crusio, and H.P. Lipp Knockout mice: simple solutions to the problems of genetic background and flanking genes Trends Neurosci. 25 2002 336 340