Dynamic changes in glypican-1 expression in dorsal root ganglion neurons after peripheral and central axonal injury

European Journal of Neuroscience

Volumn 19, Issue 5, 2004, Pages 1119-1132

  Bloechlinger, Stefan ^a   Karchewski, Laurie A ^a,b   Woolf, Clifford J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Adult; Dorsal column; DRG; Growth; Heparan sulphate proteoglycan; Nerve injury; Rat; Regeneration; Robo; Sensory neuron; Slit; Spinal cord

Indexed keywords

GLYPICAN; GLYPICAN 1; HEPARAN SULFATE; MESSENGER RNA; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE INDUCTION; MALE; NERVE CELL; NERVE FIBER GROWTH; NERVE TRANSECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REINNERVATION; SCIATIC NERVE; SPINAL CORD; SPINAL GANGLION; UPREGULATION;

ANIMALS; AXONS; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HEPARAN SULFATE PROTEOGLYCANS; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SCIATIC NEUROPATHY; SPINAL CORD;

EID: 1642356606     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03262.x     Document Type: Article

References (62)

1. Aldskogius, H., Arvidsson, J. & Grant, G. (1985) The reaction of primary sensory neurons to peripheral nerve injury with particular emphasis on transganglionic changes. Brain Res., 357, 27-46.
2. Bagri, A., Marin, O., Plump, A.S., Mak, J., Pleasure, S.J., Rubenstein, J.L. & Tessier-Lavigne, M. (2002) Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron, 33, 233-248.
3. Bandtlow, C.E. & Zimmermann, D.R. (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev., 80, 1267-1290.
4. Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J. & Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem., 68, 729-777.
5. Boilard, E., Bourgoin, S.G., Bernatchez, C., Poubelle, P.E. & Surette, M.E. (2003) Interaction of low molecular weight group 11A phospholipase A2 with apoptotic human T cells: role of heparan sulfate proteoglycans. Faseb J., 17, 1068-1080.
6. Bomze, H.M., Bulsara, K.R., Iskandar, B.J., Caroni, P. & Skene, J.H. (2001) Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat. Neurosci., 4, 38-43.
7. Bonneh-Barkay, D., Shlissel, M., Berman, B., Shaoul, E., Admon, A., Vlodavsky, I., Carey, D.J., Asundi, V.K., Reich-Slotky, R. & Ron, D. (1997) Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J. Biol. Chem., 272, 12415-12421.
8. Brose, K., Bland, K.S., Wang, K.H., Arnott, D., Henzel, W., Goodman, C.S., Tessier-Lavigne, M. & Kidd, T. (1999) Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell, 96, 795-806.
9. Carey, D.J., Stahl, R.C., Asundi, V.K. & Tucker, B. (1993) Processing and subcellular distribution of the Schwann cell lipid-anchored heparan sulfate proteoglycan and identification as glypican. Exp. Cell Res., 208, 10-18.
10. Carlson, S.L., Parrish, M.E., Springer, J.E., Doty, K. & Dossett, L. (1998) Acute inflammatory response in spinal cord following impact injury. Exp. Neurol., 151, 77-88.
11. Chong, M.S., Reynolds, M.L., Irwin, N., Coggeshall, R.E., Emson, P.C., Benowitz, L.I. & Woolf, C.J. (1994) GAP-43 expression in primary sensory neurons following central axotomy. J. Neurosci., 14, 4375-4384.
12. Costigan, M., Befort, K., Karchewski, L., Griffin, R.S., D'Urso, D., Allchorne, A., Sitarski, J., Mannion, J.W., Pratt, R.E. & Woolf, C.J. (2002) Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci., 3, 16.
13. De Leon, M., Welcher, A.A., Suter, U. & Shooter, E.M. (1991) Identification of transcriptionally regulated genes after sciatic nerve injury. J. Neurosci. Res., 29, 437-448.
14. Devor, M. & Govrin-Lippmann, R. (1979) Maturation of axonal sprouts after nerve crush. Exp. Neurol., 64, 260-270.
15. Devor, M., Schonfeld, D., Seltzer, Z. & Wall, P.D. (1979) Two modes of cutaneous reinnervation following peripheral nerve injury. J. Comp. Neurol., 185, 211-220.
16. Dusart, I. & Schwab, M.E. (1994) Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci., 6, 712-724.
17. Fransson, L.A. (2003) Glypicans. Int. J. Biochem. Cell Biol., 35, 125-129.
18. Frei, E., Klusman, I., Schnell, L. & Schwab, M.E. (2000) Reactions of oligodendrocytes to spinal cord injury: cell survival and myelin repair. Exp. Neurol., 163, 373-380.
19. Frey, D., Laux, T., Xu, L., Schneider, C. & Caroni, P. (2000) Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J. Cell Biol., 149, 1443-1454.
20. Hagino, S., Iseki, K., Mori, T., Zhang, Y., Hikake, T., Yokoya, S., Takeuchi, M., Hasimoto, H., Kikuchi, S. & Wanaka, A. (2003a) Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia, 42, 130-138.
21. Hagino, S., Iseki, K., Mori, T., Zhang, Y., Sakai, N., Yokoya, S., Hikake, T., Kikuchi, S. & Wanaka, A. (2003b) Expression pattern of glypican-1 mRNA after brain injury in mice. Neurosci. Lett., 349, 29-32.
22. Halfter, W. (1993) A heparan sulfate proteoglycan in developing avian axonal tracts. J. Neurosci., 13, 2863-2873.
23. Herndon, M.E., Stipp, C.S. & Lander, A.D. (1999) Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding. Glycobiology, 9, 143-155.
24. Himes, B.T. & Tessler, A. (1989) Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. J. Comp. Neurol., 284, 215-230.
25. Hu, H. (2001) Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci., 4, 695-701.
26. Inatani, M., Irie, F., Plump, A.S., Tessier-Lavigne, M. & Yamaguchi, Y. (2003) Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science, 302, 1044-1046.
27. Ishihara, M., Fedarko, N.S. & Conrad, H.E. (1987) Involvement of phosphatidylinositol and insulin in the coordinate regulation of proteoheparan sulfate metabolism and hepatocyte growth. J. Biol. Chem., 262, 4708-4716.
28. Jenkins, R. & Hunt, S.P. (1991) Long-term increase in the levels of c-jun mRNA and jun protein-like immunoreactivity in motor and sensory neurons following axon damage. Neurosci. Lett., 129, 107-110.
29. Jenkins, R., McMahon, S.B., Bond, A.B. & Hunt, S.P. (1993) Expression of c-Jun as a response to dorsal root and peripheral nerve section in damaged and adjacent intact primary sensory neurons in the rat. Eur. J. Neurosci., 5, 751-759.
30. Karchewski, L.A., Kim, F.A., Johnston, J., McKnight, R.M. & Verge, V.M. (1999) Anatomical evidence supporting the potential for modulation by multiple neurotrophins in the majority of adult lumbar sensory neurons. J. Comp. Neurol., 413, 327-341.
31. Karthikeyan, L., Flad, M., Engel, M., Meyer-Puttlitz, B., Margolis, R.U. & Margolis, R.K. (1994) Immunocytochemical and in situ hybridization studies of the heparan sulfate proteoglycan, glypican, in nervous tissue. J. Cell Sci., 107, 3213-3222.
32. Kenney, A.M. & Kocsis, J.D. (1997) Temporal variability of jun family transcription factor levels in peripherally or centrally transected adult rat dorsal root ganglia. Brain Res. Mol Brain Res., 52, 53-61.
33. Kenney, A.M. & Kocsis, J.D. (1998) Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia In vivo. J. Neurosci., 18, 1318-1328.
34. Li, M., Shibata, A., Li, C., Braun, P.E., McKerracher, L., Roder, J., Kater, S.B. & David, S. (1996) Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J. Neurosci. Res., 46, 404-414.
35. Liang, Y., Annan, R.S., Carr, S.A., Popp, S., Mevissen, M., Margolis, R.K. & Margolis, R.U. (1999) Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J. Biol. Chem., 274, 17885-17892.
36. Liang, Y., Haring, M., Roughley, P.J., Margolis, R.K. & Margolis, R.U. (1997) Glypican and biglycan in the nuclei of neurons and glioma cells: presence of functional nuclear localization signals and dynamic changes in glypican during the cell cycle. J. Cell Biol., 139, 851-864.
37. Lieberman, A.R. (1971) The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol., 14, 49-124.
38. Litwack, E.D., Ivins, J.K., Kumbasar, A., Paine-Saunders, S., Stipp, C.S. & Lander, A.D. (1998) Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev Dyn, 211, 72-87.
39. Litwack, E.D., Stipp, C.S., Kumbasar, A. & Lander, A.D. (1994) Neuronal expression of glypican, a cell-surface glycosylphosphatidylinositol- anchored heparan sulfate proteoglycan, in the adult rat nervous system. J. Neurosci., 14, 3713-3724.
40. Malave, C., Villegas, G.M., Hernandez, M., Martinez, J.C., Castillo, C., Suarez de Mata, Z. & Villegas, R. (2003) Role of glypican-1 in the trophic activity on PC12 cells induced by cultured sciatic nerve conditioned medium: identification of a glypican-1-neuregulin complex. Brain Res., 983, 74-83.
41. McKerracher, L., David, S., Jackson, D.L., Kottis, V., Dunn, R.J. & Braun, P.E. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron, 13, 805-811.
42. Moon, L.D., Asher, R.A., Rhodes, K.E. & Fawcett, J.W. (2002) Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience, 109, 101-117.
43. Moore, K.A., Kohno, T., Karchewski, L.A., Scholz, J., Baba, H. & Woolf, C.J. (2002) Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci., 22, 6724-6731.
44. Neumann, S. & Woolf, C.J. (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron, 23, 83-91.
45. Nguyen Ba-Charvet, K.T., Brose, K., Marillat, V., Kidd, T., Goodman, C.S., Tessier-Lavigne, M., Sotelo, C. & Chedotal, A. (1999) Slit2-Mediated chemorepulsion and collapse of developing forebrain axons. Neuron, 22, 463-473.
46. Richardson, P.M. & Issa, V.M. (1984) Peripheral injury enhances central regeneration of primary sensory neurones. Nature, 309, 791-793.
47. Ronca, F., Andersen, J.S., Paech, V. & Margolis, R.U. (2001) Characterization of Slit protein interactions with glypican-1. J. Biol. Chem., 276, 29141-29147.
48. Samad, T.A., Moore, K.A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J.V. & Woolf, C.J. (2001) Interleukin-1 beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature, 410, 471-475.
49. Schnell, L. & Schwab, M.E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature, 343, 269-272.
50. Schwab, M.E. & Bartholdi, D. (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev., 76, 319-370.
51. Schwaiger, F.W., Hager, G., Schmitt, A.B., Horvat, A., Streif, R., Spitzer, C., Gamal, S., Breuer, S., Brook, G.A., Nacimiento, W. & Kreutzberg, G.W. (2000) Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). Eur. J. Neurosci., 12, 1165-1176.
52. Skene, J.H., Jacobson, R.D., Snipes, G.J., McGuire, C.B., Norden, J.J. & Freeman, J.A. (1986) A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science, 233, 783-786.
53. Smith, D.S. & Skene, J.H. (1997) A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci., 17, 646-658.
54. Steinfeld, R., Van Den Berghe, H. & David, G. (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol., 133, 405-416.
55. Strittmatter, S.M., Fankhauser, C., Huang, P.L., Mashimo, H. & Fishman, M.C. (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell, 80, 445-452.
56. Tsujino, H., Kondo, E., Fukuoka, T., Dai, Y., Tokunaga, A., Miki, K., Yonenobu, K., Ochi, T. & Noguchi, K. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell Neurosci., 15, 170-182.
57. Wang, K.H., Brose, K., Arnott, D., Kidd, T., Goodman, C.S., Henzel, W. & Tessier-Lavigne, M. (1999) Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell, 96, 771-784.
58. Wang, H., Sun, H., Della Penna, K., Benz, R.J., Xu, J., Gerhold, D.L., Holder, D.J. & Koblan, K.S. (2002) Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience, 114, 529-546.
59. Woolf, C.J., Reynolds, M.L., Molander, C., O'Brien, C., Lindsay, R.M. & Benowitz, L.I. (1990) The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience, 34, 465-478.
60. Xiao, H.S., Huang, Q.H., Zhang, F.X., Bao, L., Lu, Y.J., Guo, C., Yang, L., Huang, W.J., Fu, G., Xu, S.H., Cheng, X.P., Yan, Q., Zhu, Z.D., Zhang, X., Chen, Z., Han, Z.G. & Zhang, X. (2002) Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc. Natl Acad. Sci. USA, 99, 8360-8365.
61. Zhang, Z., Coomans, C. & David, G. (2001) Membrane heparan sulfate proteoglycan-supported FGF2-FGFR1 signaling: evidence in support of the 'cooperative end structures' model. J. Biol. Chem., 276, 41921-41929.
62. Zou, Y., Stoeckli, E., Chen, H. & Tessier-Lavigne, M. (2000) Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell, 102, 363-375.