Identification of versican as an isolectin B4-binding glycoprotein from mammalian spinal cord tissue

FEBS Journal

Volumn 272, Issue 5, 2005, Pages 1090-1102

  Bogen, Oliver ^a   Dreger, Mathias ^a,c   Gillen, Clemens ^b   Schröder, Wolfgang ^b   Hucho, Ferdinand ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b GRÜNENTHAL GMBH   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Extracellular matrix; IB4; Neuropathic pain; Nonpeptidergic C fibers; Versican

Indexed keywords

BINDING PROTEIN; GLYCOPROTEIN; HYALURONIDASE; IMMUNOGLOBULIN; LAMININ; LECTIN; PROTEOGLYCAN; VERSICAN;

AFFINITY CHROMATOGRAPHY; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; EXTRACELLULAR MATRIX; IMMUNOPRECIPITATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NOCICEPTIVE RECEPTOR; NONHUMAN; PAIN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SPINAL CORD; SWINE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, AFFINITY; GLYCOPROTEINS; HYALURONOGLUCOSAMINIDASE; LECTINS; LECTINS, C-TYPE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEOCHONDROITIN SULFATES; PROTEOGLYCANS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPINAL CORD; SUBCELLULAR FRACTIONS; SWINE; VERSICANS;

EID: 14644409820     PISSN: 1742464X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04543.x     Document Type: Article

References (44)

1. Julius D & Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413, 203-210.
2. Streit WJ, Schulte BA, Balentine DJ & Spicer SS (1985) Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J Histochem Cytochem 33, 1042-1052.
3. Silverman JD & Kruger L (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 19, 789-801.
4. Hayes CE & Goldstein IJ (1974) An alpha-D-galactosyl-binding lectin from Bandeiraea simplicifolia seeds. Isolation by affinity chromatography and characterization. J Biol Chem 249, 1904-1914.
5. Bennett GJ & Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107.
6. Kim SH & Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50, 355-363.
7. Wang R, Guo W, Ossipov MH, Vanderah TW, Porreca F & Lai J (2003) Glial cell line-derived neurotrophic factor normalizes neurochemical changes in injured dorsal root ganglion neurons and prevents the expression of experimental neuropathic pain. Neuroscience 121, 815-824.
8. Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, Mcmahon SB & Priestley JV (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18, 3059-3072.
9. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN & Mcmahon SB (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science 290, 124-127.
10. Li L & Zhou XF (2001) Pericellular Griffonia simplicifolia I isolectin B4-binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats. J Comp Neurol 439, 259-274.
11. Amir R & Devor M (2000) Functional cross-excitation between afferent A- and C-neurons in the dorsal root ganglia. Neuroscience 95, 189-195.
12. Streit WJ, Schulte BA, Balentine JD & Spicer SS (1986) Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res 377, 1-17.
13. Gerke MB & Plenderleith MB (2004) Ultrastructural analysis of the central terminals of primary sensory neurones labelled by transganglionic transport of Bandeiraea simplicifolia I-isolectin B4. Neuroscience 127, 165-175.
14. Schmid K & Schmitt R (1976) Raffinose metabolism in Escherichia coli K12. Purification and properties of a new alpha-galactosidase specified by a transmissible plasmid. Eur J Biochem 67, 95-104.
15. Luo Y, Wen J, Luo C, Cummings RD & Cooper DK (1999) Pig xenogeneic antigen modification with green coffee bean alpha-galactosidase. Xenotransplantation 6, 238-248.
16. Fullmer JM, Riedl MS, Higgins L & Elde R (2004) Identification of some lectin IB4 binding proteins in rat dorsal root ganglia. Neuroreport 15, 1705-1709.
17. Lebaron RG, Zimmermann DR & Ruoslahti E (1992) Hyaluronate binding properties of versican. J Biol Chem 267, 10003-10010.
18. Asher R, Perides G, Vanderhaeghen JJ & Bignami A (1991) Extracellular matrix of central nervous system white matter: demonstration of an hyaluronate-protein complex. J Neurosci Res 28, 410-421.
19. Westling J, Gottschall PE, Thompson VP, Cockburn A, Perides G, Zimmermann DR & Sandy JD (2004) ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate-binding protein. Biochem J 377, 787-795.
20. Perides G, Asher RA, Lark MW, Lane WS, Robinson RA & Bignami A (1995) Glial hyaluronate-binding protein: a product of metalloproteinase digestion of versican? Biochem J 312, 377-384.
21. Zimmermann DR & Ruoslahti E (1989) Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 8, 2975-2981.
22. Shibata S, Peters BP, Roberts DD, Goldstein IJ & Liotta LA (1982) Isolation of laminin by affinity chromatography on immobilized Griffonia simplicifolia 1 lectin. FEBS Lett 142, 194-198.
23. Dours-Zimmermann MT & Zimmermann DR (1994) A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican. J Biol Chem 269, 32992-32998.
24. Ito K, Shinomura T, Zako M, Ujita M & Kimata K (1995) Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J Biol Chem 270, 958-965.
25. Zako M, Shinomura T, Ujita M, Ito K & Kimata K (1995) Expression of PG-M (V3), an alternatively spliced form of PG-M without a chondroitin sulfate attachment in region in mouse and human tissues. J Biol Chem 270, 3914-3918.
26. Lemire JM, Braun KR, Maurel P, Kaplan ED, Schwartz SM & Wight TN (1999) Versican/PG-M isoforms in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19, 1630-1639.
27. Wight TN (2002) Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol 14, 617-623.
28. Schmalfeldt M, Dours-Zimmermann MT, Winterhalter KH & Zimmermann DR (1998) Versican V2 is a major extracellular matrix component of the mature bovine brain. J Biol Chem 273, 15758-15764.
29. Niederost BP, Zimmermann DR, Schwab ME & Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J Neurosci 19, 8979-8989.
30. Schmalfeldt M, Bandtlow CE, Dours-Zimmermann MT, Winterhalter KH & Zimmermann DR (2000) Brain derived versican V2 is a potent inhibitor of axonal growth. J Cell Sci 113, 807-816.
31. Wu Y, Sheng W, Chen L, Dong H, Lee V, Lu F, Wong CS, Lu WY & Yang BB (2004) Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth. Mol Biol Cell 15, 2093-2104.
32. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57, 276-289.
33. Celio MR, Spreafico R, De Biasi S & Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21, 510-515.
34. Murakami T & Ohtsuka A (2003) Perisynaptic barrier of proteoglycans in the mature brain and spinal cord. Arch Histol Cytol 66, 195-207.
35. Lander C, Zhang H & Hockfield S (1998) Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 18, 174-183.
36. Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M & Hockfield S (2002) Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22, 7536-7547.
37. Hagihara K, Miura R, Kosaki R, Berglund E, Ranscht B & Yamaguchi Y (1999) Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain. J Comp Neurol 410, 256-264.
38. Dina OA, Parada CA, Yeh J, Chen X, Mccarter GC & Levine JD (2004) Integrin signaling in inflammatory and neuropathic pain in the rat. Eur J Neurosci 19, 634-642.
39. Wu Y, Chen L, Zheng PS & Yang BB (2002) Beta 1-integrin-mediated glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican. J Biol Chem 277, 12294-12301.
40. Gray EG & Whittaker VP (1962) The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat 96, 79-88.
41. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
43. Shevchenko A, Wilm M, Vorm O & Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68, 850-858.
44. Hayes NVL, Holmes FE, Roobol A, Garden MJ & Baines AJ (1997) Proteins of the neuronal cytoplasmic and membrane-associated cytoskeleton. In Neurochemistry: A Practical Approach, 2nd edn, Chapter 2 (Turner AJ & Bachelard HS, eds), pp. 39-71. Oxford University Press, Oxford.