Accumulation of chondroitin sulfate proteoglycans in the microenvironment of spinal motor neurons in amyotrophic lateral sclerosis transgenic rats

Journal of Neuroscience Research

Volumn 86, Issue 11, 2008, Pages 2512-2523

  Mizuno, Hideki ^a   Warita, Hitoshi ^a,b   Aoki, Masashi ^a   Itoyama, Yasuto ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NONE   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Chondroitin sulfate proteoglycan; Microenvironment; SOD1; Transgenic rat

Indexed keywords

ARGININE; COPPER ZINC SUPEROXIDE DISMUTASE; GLYCOPROTEIN; HISTAMINE; ISOPROTEIN; NEUROCAN; PHOSPHACAN; PROTEOCHONDROITIN SULFATE; VERSICAN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE MUTATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; MICROENVIRONMENT; MOTOR NEURON DISEASE; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SPINAL CORD; SPINAL CORD VENTRAL HORN; SYMPTOMATOLOGY; TRANSGENIC RAT; UPREGULATION; ANIMAL; BIOSYNTHESIS; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING; METABOLISM; MOTONEURON; PATHOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; TRANSGENIC ANIMAL; WESTERN BLOTTING;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ASTROCYTES; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; MOTOR NEURONS; PROTEOCHONDROITIN SULFATES; RATS; SPINAL CORD;

EID: 49349083891     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21702     Document Type: Article

References (64)

1. Ahmed Z, Shaw G, Sharma VP, Yang C, McGowan E, Dickson DW. 2007. Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J Histochem Cytochem 55:687-700.
2. Alexianu ME, Kozovska M, Appel SH. 2001. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57:1282-1289.
3. Aoki M, Ogasawara M, Matsubara Y, Narisawa K, Nakamura S, Itoyama Y, Abe K. 1993. Mild ALS in Japan associated with novel SOD mutation. Nat Genet 5:323-324.
4. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW. 2000. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438.
5. Boillee S, Vande Velde C, Cleveland DW. 2006a. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59.
6. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. 2006b. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. 2002. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640.
8. Busch SA, Silver J. 2007. The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17:120-127.
9. Chi L, Ke Y, Luo C, Li B, Gozal D, Kalyanaraman B, Liu R. 2006. Motor neuron degeneration promotes neural progenitor cell proliferation, migration, and neurogenesis in the spinal cords of amyotrophic lateral sclerosis mice. Stem Cells 24:34-43.
10. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
11. de Castro RC Jr, Burns CL, McAdoo DJ, Romanic AM. 2000. Metalloproteinase increases in the injured rat spinal cord. Neuroreport 11: 3551-3554.
12. Deguchi K, Takaishi M, Hayashi T, Oohira A, Nagotani S, Li F, Jin G, Nagano I, Shoji M, Miyazaki M, Abe K, Hub NH. 2005. Expression of neurocan after transient middle cerebral artery occlusion in adult rat brain. Brain Res 1037:194-199.
13. DeWitt DA, Silver J, Canning DR, Perry G. 1993. Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease. Exp Neurol 121:149-152.
14. DeWitt DA, Richey PL, Praprotnik D, Silver J, Perry G. 1994. Chondroitin sulfate proteoglycans are a common component of neuronal inclusions and astrocytic reaction in neurodegenerative diseases. Brain Res 656:205-209.
15. Faissner A, Heck N, Dobbertin A, Garwood J. 2006. DSD-1-proteoglycan/ phosphacan and receptor protein tyrosine phosphatase-beta isoforms during development and regeneration of neural tissues. Adv Exp Med Biol 557:25-53.
16. Gadomski R, Chrapusta SJ, Wojda R, Grieb P. 2006. Morphological changes and selective loss of motoneurons in the lumbar part of the spinal cord in a rat model of familial amyotrophic lateral sclerosis (fALS). Fol Neuropathol 44:154-161.
17. Gage FH. 2000. Mammalian neural stem cells. Science 287:1433-1438.
18. Galtrey CM, Fawcett JW. 2007. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1-18.
19. Gris P, Tighe A, Levin D, Sharma R, Brown A. 2007. Transcriptional regulation of scar gene expression in primary astrocytes. Glia 55:1145-1155.
20. Guan YJ, Wang X, Wang HY, Kawagishi K, Ryu H, Huo CF, Shimony EM, Kristal BS, Kuhn HG, Friedlander RM. 2007. Increased stem cell proliferation in the spinal cord of adult amyotrophic lateral sclerosis transgenic mice. J Neurochem 102:1125-1138.
21. Gurney ME, Pu H, Chin AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, et al. 1994. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772-1775.
22. Hall ED, Oostveen JA, Gurney ME. 1998. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23:249-256.
23. Haverkamp LJ, Appel V, Appel SH. 1995. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain 118:707-719.
24. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH. 2000. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20: 2218-2228.
25. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. 2006. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci 26:7405-7415.
26. Ikegami T, Nakamura M, Yamane J, Katoh H, Okada S, Iwanami A, Watanabe K, Ishii K, Kato F, Fujita H, Takahashi T, Okano HJ, Toyama Y, Okano H. 2005. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur J Neurosci 22:3036-3046.
27. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
28. Jones LL, Yamaguchi Y, Stallcup WB, Tuszynski MH. 2002. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 22:2792-2803.
29. Kabashi E, Durham HD. 2006. Failure of protein quality control in amyotrophic lateral sclerosis. Biochim. Biophys Acta 1762:1038-1050.
30. Katoh-Semba R, Matsuda M, Watanabe E, Maeda N, Oohira A. 1998. Two types of brain chondroitin sulfate proteoglycan: their distribution and possible functions in the rat embryo. Neurosci Res 31:273-282.
31. Kearns SM, Laywell ED, Kukekov VK, Steindler DA. 2003. Extracellular matrix effects on neurosphere cell motility. Exp Neurol 182:240-244.
32. Liu J, Dalmau J, Szabo A, Rosenfeld M, Huber J, Furneaux H. 1995. Paraneoplastic encephalomyelitis antigens bind to the AU-rich elements of mRNA. Neurology 45:544-550.
33. Liu Z, Martin LJ. 2006. The adult neural stem and progenitor cell niche is altered in amyotrophic lateral sclerosis mouse brain. J Comp Neurol 497:468-488.
34. Matsui F, Watanabe E, Oohira A. 1994. Immunological identification of two proteoglycan fragments derived from neurocan, a brain-specific chondroitin sulfate proteoglycan. Neurochem Int 25:425-431.
35. Matsui F, Kawashima S, Shuo T, Yamauchi S, Tokita Y, Aono S, Keino H, Oohira A. 2002. Transient expression of juvenile-type neurocan by reactive astrocytes in adult rat brains injured by kainate-induced seizures as well as surgical incision. Neuroscience 112:773-781.
36. Matsumoto A, Okada Y, Nakamichi M, Nakamura M, Toyama Y, Sobue G, Nagai M, Aoki M, Itoyama Y, Okano H. 2006. Disease progression of human SOD1 (G93A) transgenic ALS model rats. J Neurosci Res 83:119-133.
37. McKeon RJ, Schreiber RC, Rudge JS, Silver J. 1991. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
38. McKeon PJ, Jurynec MJ, Buck CR. 1999. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 19:10778-10788.
39. Meyer-Puttlitz B, Milev P, Junket E, Zimmer I, Margolis RU, Margolis RK. 1995. Chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of nervous tissue: developmental changes of neurocan and phosphacan. J Neurochem 65:2327-2337.
40. Moon LD, Asher RA, Rhodes KE, Fawcett JW. 2001. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 4:465-466.
41. Moon LD, Asher RA, Rhodes KE, Fawcett JW. 2002. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109:101-117.
42. Muir EM, Adcock KH, Morgenstern DA, Clayton R, von Stillfried N, Rhodes K, Ellis C, Fawcett JW, Rogers JH. 2002. Matrix metalloproteases and their inhibitors are produced by overlapping populations of activated astrocytes. Brain Res Mol Brain Res 100:103-117.
43. Nagai M, Aoki M, Miyoshi I, Kato M, Pasinelli P, Kasai N, Brown RH Jr, Itoyama Y. 2001. Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J Neurosci 21:9246-9254.
44. Neusch C, Bahr M, Schneider-Gold C. 2007. Glia cells in amyotrophic lateral sclerosis: new clues to understanding an old disease? Muscle Nerve 35:712-724.
45. Okamoto M, Sakiyama J, Mori S, Kurazono S, Usui S, Hasegawa M, Oohira A. 2003. Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycans neurocan and phosphacan in the limbic structures. Exp Neurol 184:179-195.
46. Pegram CN, Eng LF, Wikstrand CJ, McComb RD, Lee YL, Bigner DD. 1985. Monoclonal antibodies reactive with epitopes restricted to glial fibrillary acidic proteins of several species. Neurochem Pathol 3: 119-138.
47. Perry MJ, Lawson SN. 1993. Neurofilaments in rat and cat spinal cord; a comparative immunocytochemical study of phosphorylated and non-phosphorylated subunits. Cell Tissue Res 272:249-256.
48. Rauch U, Gao P, Janetzko A, Flaccus A, Hilgenberg L, Tekotte H, Margolis RK, Margolis RU. 1991. Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J Biol Chem 266:14785-14801.
49. Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DF, Wilcox HM, Flood DG, Beal MF, Brown RH Jr, Scott RW, Snider WD. 1996. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 13:43-47.
50. Rhodes KE, Fawcett JW. 2004. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat 204:33-48.
51. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, et al. 1993. Mutations in Cu/ Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
52. Rosenberg GA. 1995. Matrix metalloproteinases in brain injury. J Neurotrauma 12:833-842.
53. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
54. Sobel RA, Ahmed AS. 2001. White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis. J Neuropathol Exp Neurol 60:1198-1207.
55. Softoniew MV. 2005. Reactive astrocytes in neural repair and protection. Neuroscientist 11:400-407.
56. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H. 2007. Intracellular translocation of glutathione S-transferase pi during oligodendrocyte differentiation in adult rat cerebral cortex in vivo. Neuroscience (in press).
57. Tang X, Davies JE, Davies SJ. 2003. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 71:427-444.
58. Tansey FA, Cammer W. 1991. A pi form of glutathione-S-transferase is a myelin- and oligodendrocyte-associated enzyme in mouse brain. J Neurochem 57:95-102.
59. Thou N, Haas CA, Rauch U, Merten T, Fassler R, Frotscher M, Deller T. 2000. The chondroitin sulphate proteoglycan brevican is upregulated by astrocytes after entorhinal cortex lesions in adult rats. Eur J Neurosci 12:2547-2558.
60. Viapiano MS, Matthews RT. 2006. From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology. Trends Mol Med 12:488-496.
61. Vitellaro-Zuccarello L, Bosisio P, Mazzetti S, Monti C, De Biasi S. 2007. Differential expression of several molecules of the extracellular matrix in functionally and developmentally distinct regions of rat spinal cord. Cell Tissue Res 327:433-447.
62. Warita H, Murakami T, Manabe Y, Sato K, Hayashi T, Seki T, Abe K. 2001. Induction of polysialic acid-neural cell adhesion molecule in surviving motoneurons of transgenic amyotrophic lateral sclerosis mice. Neurosci Lett 300:75-78.
63. Watanabe M, Dykes-Hoberg M, Culotta VC, Price DL, Wong PC, Rothstein JD. 2001. Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol Dis 8:933-941.
64. Yoshiyama Y, Asahina M, Hattori T. 2000. Selective distribution of matrix metalloproteinase-3 (MMP-3) in Alzheimer's disease brain. Acta Neuropathol 99:91-95.