Immunocytological localization of the HNK-1 carbohydrate in murine cerebellum, hippocampus and spinal cord using monoclonal antibodies with different epitope specificities
Tóm tắt
The HNK-1 carbohydrate, an unusual 3′-sulfated glucuronic acid epitope characteristic of many neural recognition molecules, serves as a ligand in neural cell interactions and is differentially expressed in the quadriceps and saphenous branches of the femoral nerve in the PNS of adult mice. Based on these observations, we investigated the possibility that the HNK-1 carbohydrate may be differentially distributed in neurons and fiber tracts also in the CNS thereby contributing to different targeting and guidance mechanisms. We have used antibodies with different HNK-1 epitope specificities to probe for subtle differences in expression patterns. In the adult mouse cerebellum the HNK-1 carbohydrate is detectable in stripe-like compartments in the molecular and Purkinje cell layers, whereas N-CAM and its associated α2,8 polysialic acid does not show this compartmentation. In the adult hippocampus, the HNK-1 carbohydrate localizes to perineuronal nets of inhibitory interneurons and marks the inner third of the molecular layer of the dentate gyrus. In the adult spinal cord, HNK-1 labeling is most pronounced in gray matter areas. White matter enriched regions show differential labeling with regard to fiber tracts and antibody specificity. Whereas the different antibodies do not show differences in staining in the cerebellum and the hippocampus, they show differences in staining pattern of fiber tracts and motoneurons in the spinal cord. The HNK-1 expression pattern also differed in the adult spinal cord from that observed at embryonic day 14 and postnatal day 14. Our observations suggest a functional role in the specification of functionally discrete compartments in different areas of the CNS and during development.
Tài liệu tham khảo
Abo, T. & Balch, C. M. (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). Journal of Immunology 127, 1024–1029.
Altman, J. & Bayer, S. A. (1984) The development of the rat spinal cord. In Advances in Anatomy Embryology and Cell Biology (edited by Beck, F., Hild, W., van Limborgh, J., Ortmann, R., Pauly, J. E. & Schiebler, T. H.). Berlin: Springer Verlag.
Anderson, R. B. & Key, B. (1996) Expression of a novel N-CAM glycoform (NOC-1) on axon tracts in embryonic Xenopus brain. Developmental Dynamics 207, 263–269.
Anderson, R. B. & Key, B. (1999) Novel guidance cues during neuronal pathfinding in the early scaffold of axon tracts in the rostral brain. Development 126, 1859–1868.
Anderson, R. B., Walz, A., Holt, C. E. & Key, B. (1998) Chondroitin sulfates modulate axon guidance in embryonic Xenopus brain. Developmental Biology 202, 235–243.
Ariga, T., Kohriyama, T., Freddo, L., Latov, N., Saito, M., Kon, K., Ando, S., Suzuki, M., Hemling, M. E. & Rinehart, K. L. Jr., Kusunoki, S. & Yu, R. K. (1987) Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM M-proteins in patients with neuropathy. Journal of Biological Chemistry 262, 848–853.
Bakker, H., Friedmann, I., Oka, S., Kawasaki, T., NifantΈv, N., Schachner, M. & Mantei, N. (1997) Expression cloning of a cDNA encoding a sulfotransferase involved in the biosynthesis of the HNK-1 carbohydrate epitope. Journal of Biological Chemistry 272, 29942–29946.
Bansal, R., Warrington, A. E., Gard, A. L., Ranscht, B. & Pfeiffer, S. E. (1989) Multiple and novel specificities of monoclonal antibodies O1, O4, and R-mAb used in the analysis of oligodendrocyte development. Journal of Neuroscience Research 24, 548–557.
Brichta, A. M. & Grant, G. (1985) Cytoarchitectural organization of the spinal cord. In The Rat Nervous System (edited by Paxinos, G.) Vol. 2, pp. 294–309. NewYork: Academic Press.
Bronner-Fraser, M. (1986) Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Developmental Biology 115, 44–55.
Bronner-Fraser, M. (1987) Perturbation of cranial neural crest migration by the HNK-1 antibody. Developmental Biology 123, 321–331.
BrÜckner, G., Brauer, K., Hartig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girard, N., Oertel, W. H. & Reichenbach, A. (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 3, 183–200.
BrÜckner, K., Perez, L., Clausen, H. & Cohen, S. (2000) Glycosyltransferase activity of fringe modulates notch-delta interactions. Nature 406, 411–415.
Brushart, T. M. (1993) Motor axons preferentially reinnervate motor pathways. Journal of Neuroscience 13, 2730–2738.
Cajal, S. R. (1995) Histology of the nervous system (translated by Swanson, N. & Swanson, L. W.) Vol. 1, pp. 246–540. New York: Oxford University Press.
Canning, D. R. & Stern, C. D. (1988) Changes in the expression of the carbohydrate epitope HNK-1 associated with mesoderm induction in the chick embryo. Development 104, 643–655.
Chou, D. K. H., Ilyas, A. A., Evens, J. E., Costello, C., Quarles, R. H. & Jungalwala, F. B. (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. Journal of Biological Chemistry 261, 11717–11725.
Clarris, H. J. & Key, B. (2001) Expression of glycoproteins in the vomeronasal organ reveals a novel spatiotemporal pattern of sensory neuron maturation. Development 130, 1734–1743.
Cole, G. J. & Schachner, M. (1987) Localization of the L2 monoclonal antibody binding site on chicken neural cell adhesion molecule (NCAM) and evidence for its role in NCAM-mediated cell adhesion. Neuroscience Letters 78, 227–232.
Cole, G. J., Schachner, M. & Fliesler, S. J. (1988) N-linked oligosaccharides are not required for neuronneuron interactions mediated by neural cell adhesion molecule. Neuroscience Letters 93, 170–175.
Eisenman, L. M. & Hawkes, R. (1993) Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK-1 reveal a complex, overlapping molecular topography. Journal of Comparative Neurology 335, 586–605.
Frosch, M., Gorgen, I., Boulnois, G. J., Timmis, K. N. & Bitter-Suermann, D. (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proceedings of the National Academy of Sciences USA 82, 1194–1198.
Gallego, R. G., Blanco, J. L. J., Thijssen-Van Zuylen, C. W. E. M., Gotfredsen, C. H. H., Voshol, H., Duus, J. Ø., Schachner, M. & Vliegenthart, J. F. G. Epitope diversity of N-glycans from bovine peripheral myelin glycoprotein P0 revealed by mass spectrometry and nano probe MAS NMR spectroscopy. Journal of Biological Chemistry, 30834–43084.
Gennarini, G., Hirn, M., Deagostini-Bazin, H. & Goridis, C. (1984) Studies on the transmembrane disposition of the neural cell adhesion molecule N-CAM. The use of liposome-inserted radioiodinated N-CAM to study its transbilayer orientation. European Journal of Biochemistry 142, 65–73.
Gerardy-Schahn, R. & Eckhardt, M. (1994) Hot spots of antigenicity in the neural cell adhesion molecule NCAM. International Journal of Cancer 8}, 38–42.
Gerardy-Schahn, R., Eckhardt, M., Ledermann, J. & Kemshead, J. T. (1994) Topography of NCAM antigenic epitopes recognized by Sclc-cluster-1 antibodies. A consensus view. International Journal of Cancer 8, 27–29.
Griffith, L. S., Schmitz, B. & Schachner, M. (1992) L2/HNK-1 carbohydrate and protein-protein interactions mediate the homophilic binding of the neural adhesion molecule P0. Journal of Neuroscience Research 33, 639–648.
Hall, H., Liu, L., Schachner, M. & Schmitz, B. (1993) The L2/HNK-1 carbohydrate mediates adhesion of neural cells to laminin. European Journal of Neuroscience 5, 34–42.
Hicks, C., Johnston, S. H., Disibio, G., Collazo, A., Vogt, T. F. & Weinmaster, G. (2000) Fringe differentially modulates jagged1 and delta1 signalling through notch1 and notch2. Nature Cell Biology 2, 515–520.
Hiraoka, N., Nakagawa, H., Ong, E., Akama, T. O., Fukuda, M. N. & Fukuda, M. (2000) Molecular cloning and expression of two distinct human chondroitin 4-O-sulfotransferases that belong to the HNK-1 sulfotransferase gene family. Journal of Biological Chemistry 275, 20188–20196.
Hjorth-Simonsen, A. (1972) Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. Journal of Comparative Neurology 146, 219–232.
Hjorth-Simonsen, A. (1973) Some intrinsic connections of the hippocampus in the rat: An experimental analysis. Journal of Comparative Neurology 147, 145–162.
Kang, H. G., Evers, M. R., Xia, G., Baenziger, J. U. & Schachner, M. (2001) Molecular cloning and expression of an N-acetylgalactosamine-4-Osulfotransferase that transfers sulfate to terminal and non-terminal beta 1,4-linked N-acetylgalactosamine. Journal of Biological Chemistry 276, 10861–10869.
Kazemi, M., Huntenburg, C. C. & Bubbers, J. E. (1993) Lipopolysaccharide epitope specificity and binding cross reactivity of the human IgM and anti-lipid A monoclonal antibody SdJ5–1.17.15. Molecular Immunology 30, 895–902.
Keilhauer, G., Faissner, A. & Schachner, M. (1985) Differential inhibition of neuron-neuron, neuronastrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature 316, 728–730.
Kruse, J., Mailhammer, R., Wernecke, H., Faissner, A., Sommer, I., Goridis, C. & Schachner, M. (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311, 153–155.
KÜnemund, V., Jungalwala, F. B., Fischer, G., Chou, D. K., Keilhauer, G. & Schachner, M. (1988) The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions. Journal of Cell Biology 106, 213–223.
Li, J., Pearl, D. K., Pfeiffer, S. E. & Yates, A. J. (1994) Patterns of reactivity with anti-glycolipid antibodies in human primary brain tumors. Journal of Neuroscience Research 39, 148–158.
Loring, J. F. & Erickson, C. A. (1987) Neural crest cell migratory pathways in the trunk of the chick embryo. Developmental Biology 121, 220–236.
LÖw, K., Orberger, G., Schmitz, B., Martini, R. & Schachner, M. (1994) The L2/HNK-1 carbohydrate is carried by the myelin associated glycoprotein and sulfated glucuronyl glycolipids in muscle but not cutaneous nerves of adult mice. European Journal of Neuroscience 6, 1773–1781.
Luk, J. M., Lind, S. M., Tsang, R. S. & Lindberg, A. A. (1991) Epitope mapping of four monoclonal antibodies recognizing the hexose core domain of Salmonella lipopolysaccharide. Journal of Biological Chemistry 266, 23215–23225.
Martini, R., Schachner, M. & Brushart, T. M. (1994) The L2/HNK-1 carbohydrate is preferentially expressed by previously motor axon-associated Schwann cells in reinnervated peripheral nerves. Journal of Neuroscience 14, 7180–7191.
Martini, R., Xin, Y., Schmitz, B. & Schachner, M. (1992) The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves. European Journal of Neuroscience 4, 628–639.
McGarry, R. C., Helfand, S. L., Quarles, R. H. & Roder, J. C. (1983) Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 306, 376–378.
Mohan, P. S., Laitinen, J., Merenmies, J., Rauvala, H. & Jungalwala, F. B. (1992) Sulfoglycolipids bind to adhesive protein amphoterin (P30) in the nervous system. Biochemical and Biophysical Research Communications 182, 689–696.
Moloney, D. J., Panin, V. M., Johnston, S. H., Chen, J., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K. D., Haltiwanger, R. S. & Vogt, T. F. (2000) Fringe is a glycosyltransferase that modifies notch. Nature 406, 369–375.
Noronha, A. B., Ilyas, A., Antonicek, H., Schachner, M. & Quarles R. H. (1986) Molecular specificity of L2 monoclonal antibodies that bind to carbohydrate of neural adhesion molecules and their resemblance to other monoclonal antibodies recognizing the myelin-associated glycoprotein. Brain Research 385, 237–244.
Oberdick, J., Baader, S. L., Schilling, K. (1998) From zebra stripes to postal zones: Deciphering patterns of gene expression in the cerebellum. Trends in Neurosciences 21, 383–390.
Ohtsubo, K., Oka, S., Nakamura, A., Mitsumoto, S., Ono, K., LÜtjohann, J., Schachner, M., Rutishauser, U. & Kawasaki, T., submitted.
Paxinos, G. (1985) The Rat Nervous System, Vol. 2: Hindbrain and Spinal cord. Sydney: Academic Press.
Pesheva, P., Spiess, E. & Schachner, M. (1989) J1–160 and J1–180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. Journal of Cell Biology 109, 1765–1778.
Rickmann, M., Fawcett, J. W. & Keynes, R. J. (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. Journal of Embryology and Experimental Morphology 90, 437–455.
Rye, P. D., Bovin, N. V., Vlasova, E. V., Molodyk, A. A., Baryshnikov, A., Kreutz, F. T., Garinther, W. I., Schultes, B. C., Noujaim, A. A., Madiyalakan, R., Magnani, J., Nilsson, O., Nilsson, K., Nustad, K., Norum, L., Bell, H., Cao, Y., Suresh, M. R., Very, D. L., Freeman, J. V., Yeung, K. K. & Hilgers J. (1998) Summary report on the ISOBM TD-6 workshop: Analysis of 20 monoclonal antibodies against sialyl Lewisa and related antigens Montreux, Switzerland, September 19–24, 1997. Tumor Biology 19, 390–420.
Saghatelyan, A. K., Dityatev, A., Schmidt, S., Schuster, T., Bartsch, U. & Schachner, M. (2001) Reduced perisomatic inhibition, increased exitatory transmission and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Molecular and Cellular Neuroscience 17, 226–240.
Saghatelyan, A. K., Gorissen, S., Albert, M., Hertlein, B., Schachner, M. & Dityatev, A. (2000) The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA 1 region of the hippocampus. European Journal of Neuroscience 12, 3331–3342.
Sasaki, T. & Endo, T. (1999) Evidence for the presence of N-CAM 180 on astrocytes from rat cerebellum and differences in glycan structures betweenN-CAM120 and N-CAM 140. Glia 28, 236–243.
Schachner, M. & Martini, R. (1995) Glycans and the modulation of neural-recognition molecule function. Trends in Neurosciences 18, 183–191.
Schwarting, G. A., Jungalwala, F. B., Chou, D. K., Boyer, A. M. & Yamamoto, M. (1987). Sulfated glucuronic acid-containing glycoconjugates are temporally and spatially regulated antigens in the developing mammalian nervous system. Developmental Biology 120, 65–76.
Senn, C., Kutsche, M., Saghatelyan, A., Fentrop, N., BÖsl, M. R., LÖhler, J., Bartsch, U. & Schachner, M., submitted.
Sidman, R. L., Angevine, J. B. & Taber pierce, E. (1971) Atlas of the Mouse Brain and Spinal Cord. Cambridge, MA: Harvard University Press.
Takamatsu, K., Auerbach, B., Gerardyschahn, R., Eckhardt, M., Jaques, G. & Madry, N. (1994) Chacterization of tumor-associated neural cell adhesion molecule in human sperm. Cancer Research 45, 2598–2603.
Vincent, M., Duband, J. L. & Thiery, J. P. (1983) A cell surface determinant expressed early on migrating avian neural crest cells. Brain Research 285, 235–238.
Voshol, H., Van-Zuylen, C. W., Orberger, G., Vliegenthart, J. F. & Schachner, M. (1996) Structure of the HNK-1 carbohydrate epitope on bovine peripheral myelin glycoprotein P0. Journal of Biological Chemistry 271, 22957–22960.
Weber, P., Bartsch, U., Rasband, M. N., Czaniera, R., Lang, Y., Bluethmann, H., Margolis, R. U., Levinson, S. R., Shrager, P., Montag, D. & Schachner, M. (1999). Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. Journal of Neuroscience 19, 4245–4262.
Xia, G., Evers, M. R., Kang, H. G., Schachner, M. & Baenziger, J. U. (2000) Molecular cloning and expression of the pituitary glycoprotein hormone N–acetylgalactosamine-4-O–sulfotransferase. Journal of Biological Chemistry 275, 38402–38409.
Yamauchi, S., Mita, S., Matsubara, T., Fukuta, M., Habuchi. H., Kimata, K. & Habuchi, O. (2000) Molecular cloning and expression of chondroitin 4-sulfotransferase. Journal of Biological Chemistry 275, 8975–8981.
Yoshihara, Y., Oka, S., Ikeda, J. & Mori, K. (1991a) Immunoglobulin superfamily molecules in the nervous system. Neuroscience Research 10, 83–105.
Yoshihara, Y., Oka, S., Watanabe, Y. & Mori, K. (1991b) Developmentally and spatially regulated expression of HNK-1 carbohydrate antigen on a novel phosphatidylinositol-anchored glycoprotein in rat brain. Journal of Cell Biology 115, 731–744.
