Article
Full Access
Isolation and partial characterization of a cell-surface heparan sulfate proteoglycan from embryonic rat spinal cord
J. M. Guiseppetti,
J. B. McCarthy,
P. C. Letourneau,
Corresponding Author
J. M. Guiseppetti
Departments of Cell Biology and Neuroanatomy University of Minnesota, Minneapolis, Minnesota
Address reprint requests to Joanne M. Guiseppetti, Department of Cell Biology and Neuroanatomy, University of Minnesota, 4-135 Jackson Hall, 321 Church St. S. E., Minneapolis, MN 55455Search for more papers by this authorJ. B. McCarthy
Laboratory Medicine and Pathology University of Minnesota, Minneapolis, Minnesota
Biomedical Engineering Center University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorP. C. Letourneau
Departments of Cell Biology and Neuroanatomy University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorJ. M. Guiseppetti,
J. B. McCarthy,
P. C. Letourneau,
Corresponding Author
J. M. Guiseppetti
Departments of Cell Biology and Neuroanatomy University of Minnesota, Minneapolis, Minnesota
Address reprint requests to Joanne M. Guiseppetti, Department of Cell Biology and Neuroanatomy, University of Minnesota, 4-135 Jackson Hall, 321 Church St. S. E., Minneapolis, MN 55455Search for more papers by this authorJ. B. McCarthy
Laboratory Medicine and Pathology University of Minnesota, Minneapolis, Minnesota
Biomedical Engineering Center University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorP. C. Letourneau
Departments of Cell Biology and Neuroanatomy University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorAbstract
Cell-surface heparan sulfate proteoglycans (HSPGs) are potential mediators of neuronal cell adhesion, spreading, and neurite outgrowth on various extracellular matrix molecules. One possible site of HSPG attachment is a heparin binding domain of fibronectin, which is present in the synthetic peptide FN-C/H II. In this study, HSPGs extracted from embryonic rat spinal cord by detergent were purified by ionexchange chromatography, gel filtration, and affinity chromatography on an agarose column coupled with FN-C/H II conjugated to ovalbumin (OA). Heparitinase treatment of the iodinated HSPG fraction led to the appearance of a major protein core with a molecular size of 72 kDa, as determined by reducing SDS-PAGE. The intact proteoglycan has a molecular size of approximately 150–165 kDa, containing heparan sulfate glycosaminoglycan chains of about 10–15 kDa. Anti-HSPG antibodies recognized the 72 kDa core protein by immunoblotting, and stained the surface of spinal cord neurons, oligodendrocytes, and a subset of astrocytes. These results identify a cell-surface HSPG that may mediate neuron-substratum or neuron-glia interactions in embryonic central nervous system. © 1994 Wiley-Liss, Inc.
References
- Andres JL, Stanley K, Cheifetz S, Massague J (1989): Membraneanchored and soluble forms of betaglycan, a polymorphic proteoglycan that binds transforming growth factor-B. J Cell Biol 109: 3137–3145.
- Bernfield M, Hooper KC (1991): Possible regulation of FGF activity by syndecan, and integral membrane heparan sulfate proteoglycan. Ann NY Acad Sci 638: 182–194.
- Bernfield ME, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ (1992): Biology of the syndecans. Annu Rev Cell Biol 8: 1–43.
- Brelje TC, Sorenson RL (1991): Role of prolactin versus growth hormone on islet B-cell proliferation in vivo and in vitro: Implications for pregnancy. Endocrinology 128: 45–57.
- Burg M, Cole GJ (1990): Characterization of cell associated proteoglycans synthesized by embryonic neural retinal cells. Arch Bioch Biophys 276: 396–404.
- Carbonetto S, Gruver MM, Turner DC (1983): Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J Neurosci 3: 2324–2335.
- Carey DJ, Stahl RC (1990): Identification of a lipid-anchored heparan sulfate proteoglycan in Schwann cells. J Cell Biol 111: 053–2062.
- Carey DJ, Evans DM, Stahl RC, Asundi VK, Conner KJ, Garbes P, Cizmeci-Smith G (1992): Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol 117: 191–201.
- Chelberg MK, Tsilibary EC, Hauser AJ, McCarthy JB (1989): Type IV collagen-mediated melanoma cell adhesion and migration: Involvement of multiple, distinct domains of the collagen molecule. Cancer Res 49: 4796–4802.
- Cole GJ, Loewy A, Glaser L (1986): Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature 230: 445–447.
- Conrad GW, Hamilton C, Hayes E (1977): Differences in glycosaminoglycans synthesized by fibroblast-like cells from chick cornea, heart, and skin. J Biol Chem 252: 6861–6870.
- Culp LA, Laterra J, Lark MW, Beyth RJ, Tobey SL (1986): Heparan sulfate proteoglycan as mediator of some adhesive responses and cytoskeletal reorganization of cells on fibronectin matrices: Independent versus cooperative functions. In “ Functions of the Proteoglycans.” Chichester: Wiley, p. 158–183.
- Culp LA, Mugnai G, Lewandowska K, Vallen EA, Kosir MA, Houmiel KL (1989): Heparan sulfate proteoglycans of Rastransformed 3T3 of neuroblastoma cells. Ann Ny Acad Sci 556: 194–216.
- David G, Lories V, Decock B, Marynen P, Cassiman JJ, Vanden-Berghe H (1990): Molecular cloning of a phosphatidylinositolanchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J Cell Biol 111: 3165–3176.
- Dow KE, Mirski SEL, Roder JC, Riopelle RJ (1988): Neuronal proteoglycans: Biosynthesis and functional interaction with neurons in vitro. J Neurosci 8: 3278–3289.
- Dow KE, Riopelle RJ, Kisilevsky R (1991): Domains of neuronal heparan sulfate proteoglycans involved in neurite growth on laminin. Cell Tissue Res 265: 345–351.
- Drake SL, Klein DJ, Mickelson DJ, Oegema TR, Furcht LT, McCarthy JB (1992): Cell surface phosphatidylinositol-anchored heparan sulfate proteoglycan initiates mouse melanoma cell adhesion to a fibronectin-derived, heparin-binding synthetic peptide. J Cell Biol 117: 1331–1341.
- Eisenbarth GS, Walsh FS, Nirenberg M (1979): Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci USA 76: 4913–4917.
- Fok-Seang J, Miller RH (1992): Astrocyte precursors in neonatal rat spinal cord cultures. J Neurosci 12: 2751–2764.
- Gallagher JT (1989): The extended family of proteoglycans: Social residents of the pericellular zones. Curr Opin Cell Biol 1: 1201–1218.
- Gallo V, Bertolotto A, Levi G (1987): The proteoglycan chondroitin sulfate is present in a subpopulation of cultured astrocytes and in their precursors. Dev Biol 123: 282–285.
- Grumet M, Mauro V, Burgoon MP, Edelman GM, Cunningham BA (1991): Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules. J Cell Biol 113: 1399–1412.
- Haugen PK, McCarthy JB, Roche KF, Furcht LT, Letourneau PC (1992a): Central and Peripheral neurite outgrowth differs in preference for heparin-binding versus integrin binding sequences. J Neurosci 12: 2034–2042.
- Haugen PK, Letourneau PC, Drake SL, Furcht LT, McCarthy JB (1992b): A cell surface heparan sulfate proteoglycan mediates neural cell adhesion and spreading on a defined sequence from the C-terminal cell and heparin binding domain of fibronectin, FN-C/H II. J Neurosci 12: 2597–2608.
- Haugen PK, McCarthy JB, Skubitz APN, Furcht LT, Letourneau PC (1990): Recognition of the A chain carboxy-terminal heparin binding region of fibronectin involves multiple sites: two contiguous sequences act independently to promote neural cell adhesion. J Cell Biol 111: 2733–2745.
- Heinegard D, Hascall VC (1974): Characterization of chondroitin sulfate isolated from trypsin-chymotrypsin digests of cartilage proteoglycans. Arch Biochem Biophys 165: 427–441.
- Herndon ME, Lander AD (1990): A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron 4: 949–961.
- Hoffman S, Edelman GM (1987): A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc Natl Acad Sci USA 84: 2523–2527.
- Hoffman S, Crossin KL, Edelman GM (1988): Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J Cell Biol 106: 519–532.
- Hortsch M, Goodman CS (1991): Cell and substrate adhesion molecules in drosophila. Annu Rev Cell Biol 7: 505–557.
- Hynes RO, Lander AD (1992): Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68: 303–322.
- Iida J, Skubitz APN, Furcht LT, Wayner EA, McCarthy JB (1992): Coordinate role for cell surface chondroitin sulfate proteoglycan and a4B1 integrin in mediating melanoma cell adhesion to fibronectin. J Cell Biol 118: 431–444.
- Johnson-Green PC, Dow KE, Riopelle RJ (1992): Neurite growth modulation associated with astrocyte proteoglycans: Influence of activators of inflammation. Glia 5: 33–42.
- Kiefer MC, Stephans JC, Crawford K, Okino K, Barr PJ (1990): Ligand-affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc Natl Acad Sci USA 87: 6985–6989.
- Klein DJ, Brown DM, Kim Y, Oegema TR, (1986): Partial characterization of heparan and dermatan sulfate proteoglycan synthesized by normal rat glomeruli. J Biol Chem 261: 16636–16652.
- Klein DJ, Brown DM, Moran A, Oegema TR, Platt J (1989): Chondroitin sulfate proteoglycan synthesis and reutilization of B-D-xyloside-initiated chondroitin dermatan sulfate glycosaminoglycans in fetal kidney branching morphogensis. Dev Biol 133: 515–528.
- Klinger MM, Margolis RU, Margolis RK (1985): Isolation and characterization of the heparan sulfate proteoglycans of the brain. J Biol Chem 260: 4082–4090.
- Lander AD (1987): Molecules that make axons grow. Mol Neurobiol 1: 213–245.
- Lander AD (1989): Understanding the molecules of neural cell contacts: Emerging patterns of structure and function. Trends Neurosci 12: 189–195.
- Laterra J, Silbert JD, Culp LA (1983): Cell surface heparan sulfate mediates some adhesive responses to glycosaminoglycan-binding matrices, including fibronectin. J Cell Biol 96: 112–123.
- Letourneau PC, Shattuck TA (1989): Distribution and possible interactions of actin-associated proteins and cell adhesion molecules of nerve growth cones. Development 105: 505–519.
- Letourneau PC, Condic ML, Snow DM (1992): Extracellular matrix and neurite outgrowth. Curr Opin Gen Dev 2: 625–634.
- Margolis RU, Margolis RK (1989): Nervous tissue proteoglycans. Devel Neurosci 11: 278–288.
- Marynen P, Zhang J, Cassiman H, VandenBerghe H, David G (1989): Partial primary structure of the 48 and 90 kilodalton core proteins of the cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. J Biol Chem 264: 7017–7024.
- Matthew WD, Greenspan RJ, Lander AD, Reichardt LF (1985): Immunopurification and characterization of a neuronal heparan sulfate proteoglycan. J Neurosci 5: 1842–1850.
- McCarthy JB, Hagen ST, Furcht LT (1986): Human fibronectin contains distinct adhesion- and motility-promoting domains for metastatic melanoma cells. J Cell Biol 102: 179–188.
- McCarthy JB, Chelberg MK, Mickelson DJ, Furcht LT (1988): Localization and chemical synthesis of fibronectin peptides with melanoma adhesion and heparin binding activities. Biochemistry 27: 1380–1388.
- McCarthy JB, Skubitz APN, Zhao Q, Yi XY, Mickelson DJ, Klein DJ, Furcht LT (1990): RGD-independent cell adhesion to the carboxy-terminal heparin-binding fragment of fibronectin involves heparin-dependent and -independent activities. J Cell Biol 110: 777–787.
- Morris JE (1984): Isolation of the major chondroitin sulfate/dermatan sulfate and heparan sulfate proteoglycans from embryonic chick retina. Arch Biochem Biophys 235: 127–140.
- Needham LK, Adler R, Hewitt AT (1988): Proteoglycan synthesis in flat cell-free cultures of chick embryo retinal neurons and photoreceptors. Dev Biol 126: 304–314.
- Oegema TR, Hascall VC, Dziewiatkowski DD (1975): Isolation and characterization of proteoglycans from Swarn rat chondrosarcoma. J Biol Chem 250: 6151–6159.
- Oegema TR, Hascall VC, Eisenstein R (1979): Characterization of bovine aorta proteoglycan extracted with guanidine hydrochloride in the presence of protease inhibitors. J Biol Chem 254: 1312–1318.
- Raff MC, Miller RH, Noble M (1983): A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303: 390–396.
- Ranscht B, Clapshaw PA, Price J, Noble M, Seifert W (1982): Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci USA 79: 2709–2713.
- Rapraeger AC, Bernfield M (1983): Heparan sulfate proteoglycans from mouse mammary epithelial cells: A putative membrane proteoglycan associates quantitatively with lipid vesicles. J Biol Chem 258: 3632–3636.
-
Rathjen FG,
Jessell TM
(1991):
Glycoproteins that regulate the growth and guidance of vertebrate axons: Domains and dynamics of the immunoglobulin/fibronectin type III subfamily.
Semin Neurosci
3: 297–307.
10.1016/1044-5765(91)90047-R Google Scholar
- Ratner N, Bunge RP, Glaser L (1985): A neuronal cell surface heparan sulfate proteoglycan is required for dorsal root ganglion neuron stimulation of Schwann cell proliferation. J Cell Biol 101: 744–754.
- Reichardt LF, Tomaselli KJ (1991a): Extracellular matrix molecules and their receptors: Functions in neural development. Annu Rev Neurosci 14: 212–220.
- Reichardt LF, Tomaselli KJ (1991b): Regulation of neural development by the extracellular matrix. In JA McDonald, RP Mecham (eds): “ Receptors for Extracellular Matri.” New York: Academic Press, p. 157–193.
- Riopelle RJ, Dow KE (1990): Functional interactions of neuronal heparan sulfate proteoglycans with laminin. Brain Res 525: 92–100.
- Ripellino JA, Margolis RU (1989): Structural properties of the heparan sulfate proteoglycans of brain. J Neurochem 52: 807–812.
- Rogers SL, McCarthy JB, Palm SL, Furcht LT, Letourneau Pc, (1985): Neuron-specific interactions with neurite-promoting fragments of fibronectin. J Neurosci 5: 369–378.
- Rogers SL, Letourneau PC, Peterson BA, Furcht LT, McCarthy JB (1987): Selective interaction of peripheral and central nervous system cells with two distinct cell-binding domains of fibronectin. J Cell Biol 105: 1435–1442.
- Roubin R, Deagostini-Bazin H, Hirsch MR, Goridis C (1990): Modulation of NCAM expression by transforming growth factorbeta, serum and autocrine factors. J Cell Biol 111: 673–684.
- Saad B, Constam DB, Ortmann R, Moos M, Fontana A, Schachner M (1991): Astrocyte-derived TGF-B2 and NGF differentially regulate neural recognition molecule expression by cultured astrocytes. J Cell Biol 115: 473–484.
- Sanes JR (1989): Extracellular matrix molecules that influence neural development. Annu Rev Neurosci 12: 491–516.
- Saunders S, Bernfield M (1988): Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix. J Cell Biol 106: 423–430.
- Saunders S, Jalkanen M, O'Farrell S, Bernfield M (1989): Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol 108: 1547–1556.
- Sheppard AM, Hamilton SK, Pearlman AL (1991): Changes in the distribution of extracellular matrix components accompany early morphogenic events of mammalian cortical development. J Neurosci 11: 3928–3942.
- Stewart JM, Young JD (1984): “ Solid Phase Peptide Synthesis.” 2nd ed. Rockford, II.: Pierce Chemical Co.
- Takeichi M (1991): Cadherin cell adhesion receptors as a morphogenic regulator. Science 251: 1451–1455.
- Vallen EA, Eldridge KA, Culp LA (1988): Heparan sulfate proteoglycans in the substratum adhesion sites of human neuroblastoma cells: Modulation of affinity binding to fibronectin. J Cell Physiol 135: 200–212.
- Waite KA, Mugnai G, Culp LA (1987): A second cell-binding domain on fibronectin (RGDS-independent) for neurite extension of human neuroblastoma cells. Exp Cell Res 169: 311–327.
- Walicke PA (1989): Novel neurotrophic factors, receptors, and oncogenes. Annu Rev Neurosci 12: 103–126.
- Wasteson A (1971): A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulfate. J Chromatogr 59: 87–97.
- Wight TN, Kinsella MG, Qwarnstrom EE (1992): The role of proteoglycans in cell adhesion, migration and proliferation. Curr Opin Cell Biol 4: 793–801.
- Woods A, Couchman JR, Johansson S, Hook M (1986): Adhesion and cytoskeletal organization of fibroblasts in response to fibronectin fragments. EMBO J 5: 665–670.
- Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM (1991): Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64: 841–848.
- Zaremba S, Guimaraes A, Kalb RG, Hockfield S (1989): Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2: 1207–1219.
Citing Literature
