Peripheral blood mononuclear cell infiltration and neuroinflammation in the HexB-/- mouse model of neurodegeneration

Journal of Neuroimmunology

Volumn 203, Issue 1, 2008, Pages 50-57

  Kyrkanides, Stephanos ^a   Miller, Ann W ^a   Miller, Jen nie H ^a   Tallents, Ross H ^a   Brouxhon, Sabine M ^a   Olschowka, Mallory E ^a   O'Banion, M Kerry ^a   Olschowka, John A ^a  

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

Author keywords

CCR2; Chemokine receptors; Microglia; Neurodegeneration; Neuroinflammation; Peripheral blood; Sandhoff disease

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE B; CHEMOKINE RECEPTOR CCR2; GANGLIOSIDE GM2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL ACTIVATION; CELL INFILTRATION; CONTROLLED STUDY; DEATH; DISEASE COURSE; DISEASE MODEL; ENCEPHALITIS; GM2 GANGLIOSIDOSIS; IMMUNOCOMPETENT CELL; KNOCKOUT MOUSE; MACROPHAGE; MICROGLIA; MONOCYTE; MOUSE; NERVE DEGENERATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SANDHOFF DISEASE;

ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; ENCEPHALITIS; FEMALE; G(M2) GANGLIOSIDE; HEXOSAMINIDASE B; LEUKOCYTES, MONONUCLEAR; MALE; MICE; MICE, KNOCKOUT; MICROGLIA; NERVE DEGENERATION; RECEPTORS, CCR2; SANDHOFF DISEASE;

EID: 52949130599     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.06.024     Document Type: Article

References (34)

1. Babcock A.A., Kuziel W.A., Rivest S., and Owens T. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J. Neurosci. 23 (2003) 7922-7930
2. Block M.L., Zecca L., and Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8 (2007) 57-69
3. Boring L., Gosling J., Chensue S.W., Kunkel S.L., Farese Jr. R.V., Broxmeyer H.E., and Charo I.F. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100 (1997) 2552-2561
4. Boutin H., LeFeuvre R.A., Horai R., Asano M., Iwakuraand Y., and Rothwell N.J. Role of IL-1a and IL-1b in ischemic brain damage. J. Neurosci. 21 (2001) 5528-5534
5. Carlson N.G., Wieggel W.A., Chen J., Bacchi A., Rogers S.W., and Gahring L.C. Inflammatory cytokines IL-1α, IL-1β, IL-6, and TNF-α impart neuroprotection to an excitotoxin through distinct pathways. J. Immunol. 163 (1999) 3963-3968
6. Charo I.F., and Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. New Engl. J. Med. 354 (2006) 610-621
7. Fife B.T., Huffnagle G.B., Kuziel W.A., and Karpus W.J. CC Chemokine Receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp. Med. 192 (2000) 899-906
8. Ford A.L., Goodsall A.L., Hickey W.F., and Sedgwick J.D. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4 + T cells compared. J. Immunol. 154 (1995) 4309-4321
9. Gaupp S., Pitt D., Kuziel W.A., Cannella B., and Raine C.S. Experimental autoimmune encephalomyelitis (EAE) in CCR2(-/-) mice: susceptibility in multiple strains. Am..J. Pathol. 162 (2003) 139-150
10. Griffin W.S.T., Stanley L.C., Ling C., White L., MacLeod V., Perrot L.J., White C.L., and Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 7611-7615
11. Griffin W.S.T., Sheng J.G., Robertsand G.W., and Mrak R.E. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J. Neuropath. Exp. Neurol. 54 (1995) 276-281
12. Huang D.R., Wang J., Kivisakk P., Rollins B.J., and Ransohoff R.M. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193 (2001) 713-726
13. Izikson L., Klein R.S., Charo I.F., Weiner H.L., and Luster A.D. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J. Exp. Med. 192 (2000) 1075-1080
14. Jeyakumar M., Thomas R., Elliot-Smith E., Smith D.A., van der Spoel A.C., d'Azzo A., Perry V.H., Butters T.D., Dwek R.A., and Platt F.M. Central nervous system inflammation is a hallmark of pathogenesis in mouse models of GM1 and GM2 gangliosidosis. Brain 126 Pt 4 (2003) 974-987
15. Khoury J.E., Toft M., Hickman S.E., Means T.K., Terada K., Geula C., and Luster A.D. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13 (2007) 432-438
16. Kyrkanides S., Miller J.H., Brouxhon S.M., Olschowka J.A., and Federoff H.J. β-hexosaminidase lentiviral vectors: transfer into the CNS via systemic administration. Brain Res. Mol. Brain Res. 133 (2005) 286-298
17. Kyrkanides S., Miller J.N., Tallents R.H., Brouxhon S.M., Centola G.M., and Olschowka J.A. Intraperitoneal inoculation of Sandhoff mouse neonates with an HIV-1 based lentiviral vector exacerbates the attendant neuroinflammation and disease phenotype. J. Neuroimmunol. 188 (2007) 39-47
18. Li R., Yang L., Lindholm K., Konishi Y., Yue X., Hampel H., Zhang D., and Shen Y. Tumor necrosis factor death receptor signaling cascade is required for amyloid-β protein-induced neuron death. J. Neurosci. 24 (2004) 1760-1771
19. Mahad D., Callahan M.K., Williams K.A., Ubogu E.E., Kivisakk P., Tucky B., Kidd G., Kingsbury G.A., Chang A., Fox R.J., Mack M., Sniderman M.B., Ravid R., Staugaitis S.M., Stins M.F., and Ransohoff R.M. Modulating CCR2 and CCL2 at the blood-brain barrier: relevance for multiple sclerosis pathogenesis. Brain 129 Pt 1 (2006) 212-223
20. Mason J.L., Suzuki K., Chaplin D.D., and Matsushima G.K. Interleukin-1β promotes repair of the CNS. J. Neurosci. 21 (2001) 7046-7052
21. Mrak R.E., Shengand J.G., and Griffin W.S. Glial cytokines in Alzheimer's disease: review and pathogenic implications. Hum. Pathol. 26 (1995) 816-823
22. Myerowitz R., Lawson D., Mizukami H., Mi Y., Tifft C.J., and Proia R.L. Molecular pathophysiology in Tay-Sachs and Sandhoff diseases as revealed by gene expression profiling. Hum. Mol. Genet. 11 (2002) 1343-1350
23. Norflus F., Tifft C.J., McDonald M.P., Goldstein G., Crawley J.N., Hoffmann A., Sandhoff K., Suzuki K., and Proia R.L. Bone marrow transplantation prolongs life span and ameliorates neurologic manifestations in Sandhoff disease mice. J. Clin. Invest. 101 (1998) 1881-1888
24. Ohmi K., Greenberg D.S., Rajavel K.S., Ryazantsev S., Li H.H., and Neufeld E.F. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 1902-1907
25. Rottman J.B., Slavin A.J., Silva R., Weiner H.L., Gerard C.G., and Hancock W.W. Leukocyte recruitment during onset of experimental allergic encephalomyelitis is CCR1 dependent. Eur. J. Immunol. 30 (2000) 2372-2377
26. Sango K., Yamanaka S., Hoffman A., Okuda Y., Grinberg A., Westphal H., McDonald M.P., Crawley J.N., Sandhoff K., Suzuki K., and Proia R.L. Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nature Genet 11 (1995) 170-176
27. Sango K., McDonald M.P., Crawley J.N., Mack M.L., Tifft C.J., Skop E., Starr C.M., Hoffmann A., Sandhoff K., Suzuki K., and Proia R.L. Mice lacking both subunits of lysosomal beta-hexosaminidase display gangliosidosis and mucopolysaccharidosis. Nat. Genet. 14 (1996) 348-352
28. Shaftel S.S., Kyrkanides S., Olschowka J.A., Miller J.N., Johnson R.E., and O'Banion M.K. Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J. Clin. Invest. 117 (2007) 1595-1604
29. Shaftel S.S., Carlson T.J., Olschowka J.A., Kyrkanides S., Matousek S.B., and O'Banion M.K. Chronic IL-1 expression in mouse brain leads to leukocyte infiltration and neutrophil independent blood-brain barrier permeability without overt neurodegeneration. J. Neurosci. 27 (2007) 9301-9309
30. Sedgwick J.D., Ford A.L., Foulcher E., and Airriess R. Central nervous system microglial cell activation and proliferation follows direct interaction with tissue-infiltrating T cell blasts. J. Immunol. 160 (1998) 5320-5330
31. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., and Suzumura A. Tumor necrosis factor-α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 281 (2006) 21362-21368
32. Toulmond S., and Rothwell N.J. Interleukin 1 in the brain: biology, pathology and therapeutic target. J. Neuroimmunol. 111 (2000) 1-9
33. Wada R., Tifft C.J., and Proia R.L. 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
34. Wu Y.P., and Proia R.L. Deletion of macrophage-inflammatory protein 1 alpha retards neurodegeneration in Sandhoff disease mice. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8425-8430