Abstract
Diffusely infiltrating astrocytic tumours of the central nervous system (CNS) are the most frequent intracranial neoplasms and account for more than 60% of all primary brain tumours in man. Until recently, it was generally accepted that the glial component of the mature CNS, consisted of differentiated astrocytes, ependymal cells, oligodendrocytes and the non-neuro-ectodermal microglial cells. There exists a recently recognised population of glial cells that express the NG2 proteoglycan (NG2 cells). NG2 cells are dynamic and undergo rapid morphological changes in response to a variety of CNS pathologies. They are highly motile cells, which interact with various extracellular matrix (ECM) in association with the integrin receptors. During angiogenesis and response to tissue injury, NG2 precursor cells are recruited to sites where vessel growth and repair are occurring. NG2 is over-expressed by both tumour cells and pericytes on the blood vessels of malignant brain tumours. The function of NG2 cells in the CNS, and the notion of them as a source of and/or lineage marker for some gliomas are discussed. In addition, their possible role in glioma angiogenesis, proliferation and invasion will be considered as will their value in provision of targets for clinical and pre-clinical therapeutic strategies in brain tumours.
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Akiyama, Y., Jung, S., Salhia, B., Lee, S., Hubbard, S., Taylor, M., Mainprize, T., Akaishi, K., Van Furth, W.& Rutka, J. T.(2001) J Neurooncol 53, 115–127.
Arnett, H. A., Mason, J., Marino, M., Suzuki, K.& Matsushima, G. K.(2001) Nat Neurosci 4(11), 1116–1122.
Ting, J. P. Ashley, D. M., Batra, S. K.& Bigner, D. D.(1997) J Neurooncol 35, 259–273.
Back, S. A., Luo, N. L., Borenstein, N. S., Levine, J. M., Volpe, J. J.& Kinney, H. C.(2001) J Neurosci 21, 1302–1312.
Balabanov, R.& Dore-Duffy, P.(1998) J Neurosci Res 53, 637–644.
Barnett, S. C., Robertson, L., Graham, D., Allan, D.& Rampling, R.(1998) Carcinogenesis 19, 1529–1537.
Barron, K. D.(1995) J Neuro Sci 134, 57–68.
Behm, F. G., Smith, F. O., Raimondi, S. C., Pui, C. H.& Bernstein, I. D.(1996) Blood 87, 1134–1139.
Behnke, J., Mach, J. P., Buchegger, F., Carrel, S., Delaloye, B.& De Tribolet, N.(1988) Br J Neurosurg 2, 193–197.
Berens, M. E.& Giese A.(1999) Neoplasia 1, 208–219.
Bigner, D. D., Brown, M., Coleman, R. E., Friedman, A. H., Friedman, H. S., McLendon, R. E., Bigner, S. H., Zhao, X. G., Wikstrand, C. J., Pegram, C. N. et al.(1995) J Neurooncol 24, 109–122.
Bodmer, S., Strommer, K., Frei, K., Siepl, C., De Tribolet, N., Heid, I.& Fontana, A.(1989) J Immunol 143, 3222–3229.
Boehm, T., Folkman, J., Browder, T.& O'Reilly, M. S.(1997) Nature 390, 404–407.
Bolteus, A. J., Berens, M. E.& Pilkington, G. J.(2001) Curr Neurol Neurosci Rep 1, 225–232.
Bu, J., Akhtar, N.& Nishiyama, A.(2001) Glia 34, 296–310.
Buchegger, F., Mach, J. P., Leonnard, P.& Carrel, S.(1986) Cancer 58, 655–662.
Bumol, T. F.& Reisfeld, R. A.(1982) Proc Natl Acad Sci USA 79, 1245–1249.
Bumol, T. F., Walker, L. E.& Reisfeld, R. A.(1984) J Biol Chem 259, 12733–12741.
Bumol, T. F., Wang, Q. C., Reisfeld, R. A.& Kaplan, N. O.(1983) Proc Natl Acad Sci USA 80, 529–533.
Burg, M. A., Grako, K. A.& Stallcup, W. B.(1998) J Cell Physiol 177, 299–312.
Burg, M. A., Nishiyama, A.& Stallcup, W. B.(1997) Exp Cell Res 235, 254–264.
Burg, M. A., Pasqualini, R., Arap, W., Ruoslahti, E.& Stallcup, W. B.(1999) Cancer Res 59, 2869–2874.
Burg, M. A., Tillet, E., Timpl, R.& Stallcup, W. B.(1996) J Biol Chem 271, 26110–26116.
Burrows, F. J.& Thorpe, P. E.(1993) Proc Natl Acad Sci USA 90, 8996–9000.
Butt, A. M., Duncan, A., Hornby, M. F., Kirvell, S. L., Hunter, A., Levine, J. M.& Berry, M.(1999) Glia 26, 84–91.
Carrel, S., Accolla, R. S., Carmagnola, A. L.& Mach, J. P.(1980) Cancer Res 40, 2523–2528.
Chekenya, M., Enger, P., Thorsen, F., Tysnes, B. B., Al-Sarraj, S., Read, T. A., Furmanek, T., Mahesparan, R., Levine, J. M., Butt, A. M., Pilkington, G. J.& Bjerkvig, R.(2002a) Neuropath and Applied Neurobiol 28(5), 367–380.
Chekenya, M., Hjelstuen, M., Enger, P. O., Thorsen, F., Jacob, A. L., Probst, B., Haraldseth, O., Pilkington, G., Butt, A., Levine, J. M.& Bjerkvig, R.(2002b) FASEB J(2002), Express article 10.1096/fj.01-0632fje; FASEB J(2002) 16(6); 586–816(6):586–588.
Chekenya, M., Rooprai, H. K., Davies, D., Levine, J. M., Butt, A. M.& Pilkington, G. J.(1999) Int J Dev Neurosci 17, 421–435.
Chintala, S. K., Sawaya, R., Gokaslan, Z. L., Fuller, G.& Rao, J. S.(1996) Cancer Lett 101, 107–114.
Cokgor, I., Akabani, G., Friedman, H. S., Friedman, A. H., Zalutsky, M. R., Zehngebot, L. M., Provenzale, J. M., Guy, C. D., Wikstrand, C. J.& Bigner, D. D.(2001) Cancer 91, 1809–1813.
Colapinto, E. V., Humphrey, P. A., Zalutsky, M. R., Groothuis, D. R., Friedman, H. S., De Tribolet, N., Carrel, S.& Bigner, D. D.(1988) Cancer Res 48, 5701–5707.
Colapinto, E. V., Zalutsky, M. R., Archer, G. E., Noska, M. A., Friedman, H. S., Carrel, S.& Bigner, D. D.(1990) Cancer Res 50, 1822–1827.
CUSHING (1928) Tumors Arising from the Blood-Vessels of the Brain: Angiomatous Malformations and Hemangioblastomas. Illanois: Spring-Field.
Davis, P.-M. S.(1998) Epidemiology. Incidence and survival. Arnold.
Dawson, M. R., Levine, J. M.& Reynolds, R.(2000) J Neurosci Res 61, 471–479.
De Vries, J. E., Keizer, G. D., Te Velde, A. A., Voordouw, A., Ruiter, D., Rumke, P., Spits, H.& Figdor, C. G.(1986) Int J Cancer 38, 465–473.
Diener, E., Diner, U. E., Sinha, A., Xie, S.& Vergidis, R.(1986) Science 231, 148–150.
Doane, K. J., Howell, S. J.& Birk, D. E.(1998) Invest Ophthalmol Vis Sci 39, 263–275.
Doetsch, F., Garcia-Verdugo, J. M.& Alvarezbuylla, A.(1999) Proc Natl Acad Sci USA 96, 11619–11624.
Dou, C. L.& Levine, J. M.(1994) J Neurosci 14, 7616–7628.
East, J. A., Mitchell, S. D.& Hart, I. R.(1993) Melanoma Res 3, 341–346.
Edgar, D., Timpl, R.& Thoenen, H.(1984) Embo J 3, 1463–1468.
Epenetos, A. A., Snook, D., Durbin, H., Johnson, P. M.& Taylor-Papadimitriou, J.(1986) Cancer Res 46, 3183–3191.
Epenetos, A. A., Snook, D., Hooker, G., Lavender, J. P.& Halnan, K. E.(1984) Lancet 2, 169.
Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A.& Gage, F. H.(1998) Nat Med 4, 1313–1317.
Fang, X., Burg, M. A., Barritt, D., Dahlinhuppe, K., Nishiyama, A.& Stallcup, W. B.(1999) Mol Biol Cell 10, 3373–3387.
Fawcett, J. W.& Asher, R. A.(1999) Brain Res Bull 49, 377–391.
Ferns, G. A., Raines, E. W., Sprugel, K. H., Motani, A. S., Reidy, M. A.& Ross, R.(1991) Science 253, 1129–1132.
Fidler, P. S., Schuette, K., Asher, R. A., Dobbertin, A., Thornton, S. R., Callepatino, Y., Muir, E., Levine, J. M., Geller, H. M., Rogers, J. H., Faissner, A.& Fawcett, J. W.(1999) J Neurosci 19, 8778–8788.
Fleming, T. P., Saxena, A., Clark, W. C., Robertson, J. T., Oldfield, E. H., Aaronson, S. A.& Ali, I. U.(1992) Cancer Res 52, 4550–4553.
Folkman, J.(1971) N Engl J Med 285, 1182–1186.
Folkman, J.(1995) Nat Med 1, 27–31.
Folkman, J., Watson, K., Ingber, D.& Hanahan, D.(1989) Nature 339, 58–61.
Frisen, J., Johansson, C. B., Lothian, C.& Lendahl, U.(1998) Cell Mol Life Sci 54, 935–945.
Fulton, B. P., Burne, J. F.& Raff, M. C.(1992) J Neurosci 12, 4816–4833.
Gage, F. H.(1998) Curr Opin Neurobiol 8, 671–676.
Garrigues, H. J., Lark, M. W., Lara, S., Hellstrom, I., Hellstrom, K. E.& Wight, T. N.(1986) J Cell Biol 103, 1699–1710.
Giese, A., Loo, M. A., Tran, N., Haskett, D., Coons, S. W.& Berens, M. E.(1996) Int J Cancer, 67, 275–282.
Gehrmann, J., Matsumoto, Y.& Kreutzberg, G. W.(1995) Brain Res Brain Res Rev 20, 269–287.
Giordana, M. T., Germano, I., Giaccone, G., Mauro, A., Migheli, A.& Schiffer, D.(1985) Acta Neuropathol (Berl) 67, 51–57.
Gladson, C. L.(1999) J Neuropathol Exp Neurol 58, 1029–1040.
Goldman, J. E.(2000) J Neurosci Res 59, 410–412.
Goodson, R. J., Doyle, M. V., Kaufman, S. E.& Rosenberg, S.(1994) Proc Natl Acad Sci USA 91, 7129–7133.
Goretzki, L., Burg, M. A., Grako, K. A.& Stallcup, W. B.(1999) J Biol Chem 274, 16831–16837.
Goretzki, L., Lombardo, C. R.& Stallcup, W. B.(2000) J Biol Chem 275, 28625–28633.
Gould, E., Reeves, A. J., Graziano, M. S.& Gross, C. G.(1999) Science 286, 548–552.
Gould, E., Tanapat, P., McEwen, B. S., Flugge, G.& Fuchs, E.(1998) Proc Natl Acad Sci USA 95, 3168–3171.
Grako, K. A., Ochiya, T., Barritt, D., Nishiyama, A.& Stallcup, W. B.(1999) J Cell Sci 112(Pt 6), 905–915.
Grako, K. A.& Stallcup, W. B.(1995) Exp Cell Res 221, 231–240.
Gratsa, A., Rooprai, H. K., Rogers, J. P., Martin, K. K.& Pilkington, G. J.(1997) Anticancer Res 17, 4111–4117.
Hall, A., Giese, N. A.& Richardson, W. D.(1996) Development 122, 4085–4094.
Hanahan, D., Christofori, G., Naik, P.& Arbeit, J.(1996) Eur J Cancer 32A, 2386–2393.
Harper, J. R., Bumol, T. F.& Reisfeld, R. A.(1984) J Immunol 132, 2096–2104.
Harper, J. R.& Reisfeld, R. A.(1983) J Natl Cancer Inst 71, 259–263.
Hedberg, K. M., Mahesparan, R., Read, T. A., Tysnes, B. B., Thorsen, F., Visted, T., Bjerkvig, R.& Fredman, P.(2001) Neuropathol Appl Neurobiol 27, 451–464.
Hermanson, M., Funa, K., Koopmann, J., Maintz, D., Waha, A., Westermark, B., Heldin, C. H., Wiestler, O. D., Louis, D. N., Von Deimling, A.& Nister, M.(1996) Cancer Res 56, 164–171.
Hirschi, K. K.& D'amore, P. A.(1997) Exs 79, 419–428.
Humphries, M. J.(2000) Trends Pharmacol Sci 21, 29–32.
Hwang, K. M., Fodstad, O., Oldham, R. K.& Morgan, A. C. Jr.(1985) Cancer Res 45, 4150–4155.
Iida, J., Meijne, A. M., Spiro, R. C., Roos, E., Furcht, L. T.& McCarthy, J. B.(1995) Cancer Res 55, 2177–2185.
Ito, D., Imai, Y., Ohsawa, K., Nakajima, K., Fukuuchi, Y.& Kohsaka, S.(1998) Brain Res Mol Brain Res 57, 1–9.
Jain, R. K.& Baxter, L. T.(1988) Cancer Res 48, 7022–7032.
Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U.& Frisen, J.(1999) Cell 96, 25–34.
Jones, L. L., Yamaguchi, Y., Stallcup, W. B.& Tuszynski, M. H.(2002) J Neurosci 22, 2792–2803.
Kerbel, R. S.(1991) Bioessays 13, 31–36.
Kerbel, R. S.(1997) Nature 390, 335–336.
Kleihues, P., Burger, P. C.& Scheithauer, B. W.(1993) Brain Pathol 3, 255–268.
Kleihues, P.& Cavenee. W.(2000) World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of the Nervous System. Lyon: Oxford University Press.
Kligman, D.& Hilt, D. C.(1988) Trends Biochem Sci 13, 437–443.
Koivunen, E., Arap, W., Valtanen, H., Rainisalo, A., Medina, O. P., Heikkila, P., Kantor, C., Gahmberg, C. G., Salo, T., Konttinen, Y. T., Sorsa, T., Ruoslahti, E.& Pasqualini, R.(1999a) Nat Biotechnol 17, 768–774.
Koivunen, E., Restel, B. H., Rajotte, D., Lahdenranta, J., Hagedorn, M., Arap, W.& Pasqualini, R.(1999b) Methods Mol Biol 129, 3–17.
Koivunen, E., Wang, B.& Ruoslahti, E.(1995) Biotechnology (NY) 13, 265–270.
Kokkinakis, D. M., Watson, M. L., Honig, L. S., Rushing, E. J., Mickey, B. E.& Schold, S. C. Jr.(2001) Neuro-Oncol 3, 99–112.
Koochekpour, S.& Pilkington, G. J.(1996) Cancer Lett 104, 97–102.
Kuo, H. J., Maslen, C. L., Keene, D. R.& Glanville, R. W.(1997) J Biol Chem 272, 26522–26529.
Kuppner, M. C., Van Meir, E., Gauthier, T., Hamou, M. F.& De Tribolet, N.(1992) Int J Cancer 50, 572–577.
Larsen, R. H., Akabani, G., Welsh, P.& Zalutsky, M. R.(1998) Radiat Res 149, 155–162.
Leger, O., Johnson-Leger, C., Jackson, E., Coles, B.& Dean, C.(1994) Int J Cancer 58, 700–705.
Lemmon, V., Farr, K. L.& Lagenaur, C.(1989) Neuron 2, 1597–1603.
Leong, S. K.& Ling, E. A.(1992) Glia 6, 39–47.
Levine, J. M.(1994) J Neurosci 14, 4716–4730.
Levine, J. M.& Card, J. P.(1987) J Neurosci 7, 2711–2720.
Levine, J. M., Enquist, L. W.& Card, J. P.(1998) Glia 23, 316–328.
Levine, J. M., Reynolds, R.& Fawcett, J. W.(2001) Trends Neurosci 24, 39–47.
Levine, J. M., Stincone, F.& Lee, Y. S.(1993) Glia 7, 307–321.
Levison, S. W., Young, G. M.& Goldman, J. E.(1999) J Neurosci Res 57, 435–446.
Lin, X. H., Dahlin-Huppe, K.& Stallcup, W. B.(1996) J Cell Biochem 63, 463–477.
Lindahl, P.& Betsholtz, C.(1998) Curr Opin Nephrol Hypertens 7, 21–26.
Lindahl, P., Johansson, B. R., Leveen, P.& Betsholtz, C.(1997) Science 277, 242–245.
Lindmo, T., Boven, E., Cuttitta, F., Fedorko, J.& Bunn, P. A. Jr.(1984) J Immunol Methods 72, 77–89.
Mariani, L., Beaudry, C., McDonough, W. S., Hoelzinger, D. B., Demuth, T., Ross, K. R., Berens, T., Coons, S. W., Watts, G., Trent, J. M., Wei, J. S., Giese, A.& Berens, M. E.(2001) J Neuro-Oncology 53, 161–176.
Mauvieux, L., Delabesse, E., Bourquelot, P., Radford-Weiss, I., Bennaceur, A., Flandrin, G., Valensi, F.& Macintyre, E. A.(1999) Br J Haematol 107, 674–676.
McKnight, A. J., Macfarlane, A. J., Dri, P., Turley, L., Willis, A. C.& Gordon, S.(1996) J Biol Chem 271, 486–489.
McTigue, D. M., Wei, P.& Stokes, B. T.(2001) J Neurosci 21, 3392–3400.
Merzak, A., Koocheckpour, S.& Pilkington, G. J.(1994) Cancer Res 54, 3988–3992.
Merzak, A., Koochekpour, S., McCrea, S., Roxanis, Y.& Pilkington, G. J.(1995) Mol Chem Neuropathol 24, 121–135.
Midwood, K. S.& Salter, D. M.(2001) J Pathol 195, 631–635.
Miller, B., Sheppard, A. M., Bicknese, A. R.& Pearlman, A. L.(1995) J Comp Neurol 355, 615–628.
Morgan, A. C., Jr., Galloway, D. R.& Reisfeld, R. A.(1981) Hybridoma 1, 27–36.
Murayama, O., Nishida, H.& Sekiguchi, K.(1996) J Biochem (Tokyo) 120, 445–451.
Neuwelt, E. A., Specht, H. D., Barnett, P. A., Dahlborg, S. A., Miley, A., Larson, S. M., Brown, P., Eckerman, K. F., Hellstrom, K. E.& Hellstrom, I.(1987) Neurosurgery 20, 885–895.
Nishiyama, A.(2001) Hum Cell 14, 77–82.
Nishiyama, A., Dahlin, K. J., Prince, J. T., Johnstone, S. R.& Stallcup, W. B.(1991) J Cell Biol 114, 359–371.
Nishiyama, A., Lin, X. H., Giese, N., Heldin, C. H.& Stallcup, W. B.(1996a) J Neurosci Res 43, 299–314.
Nishiyama, A., Lin, X. H., Giese, N., Heldin, C. H.& Stallcup, W. B.(1996b) J Neurosci Res 43, 315–330.
Nishiyama, A.& Stallcup, W. B.(1993) Mol Biol Cell 4, 1097–1108.
Nishiyama, A., Yu, M., Drazba, J. A.& Tuohy, V. K.(1997) J Neurosci Res 48, 299–312.
Nister, M., Libermann, T. A., Betsholtz, C., Pettersson, M., Claesson-Welsh, L., Heldin, C. H., Schlessinger, J.& Westermark, B.(1988) Cancer Res 48, 3910–3918.
Noble, A. M.-P.(2001) Glial Restricted Precursors. Totowa, New Jersey: Humana Press.
Noble, M., Murray, K., Stroobant, P., Waterfield, M. D.& Riddle, P.(1988) Nature 333, 560–562.
Orlidge, A.& D'amore, P. A.(1987) J Cell Biol 105, 1455–1462.
Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E.& Stallcup, W. B.(2001) Dev Dyn 222, 218–227.
Ozerdem, U., Monosov, E.& Stallcup, W. B.(2002) Microvasc Res 63, 129–134.
Palmer, T. D., Takahashi, J.& Gage, F. H.(1997) Mol Cell Neurosci 8, 389–404.
Paulus, W., Roggendorf, W.& Schuppan, D.(1988) Virchows Arch A Pathol Anat Histopathol 413, 325–332.
Pedersen, P. H., Marienhagen, K., Mork, S.& Bjerkvig, R.(1993) Cancer Res 53, 5158–5165.
Pennington, M. E., Lam, K. S.& Cress, A. E.(1996) Mol Divers 2, 19–28.
Pilkington, G. J.(1994) Brain Pathology 4, 157–166.
Pilkington, G. J.(1996) Brazilian Journal of Medical and Biological Research 29, 1159–1172.
Pilkington, G. J.(1992) Neuropathol Appl Neurobiol 18, 434–442.
Pilkington, G. J., Dunan, J. R., Rogers, J. P., Clarke, T. M.& Knott, J. C.(1993) Neurosci Lett 149, 1–5.
Pouly, S., Becher, B., Blain, M.& Antel, J. P.(1999) Glia 27, 259–268.
Pouly, S., Prat, A., Blain, M., Olivier, A.& Antel, J.(2001) Acta Neuropathol (Berl) 102, 313–320.
Raff, M. C., Miller, R. H.& Noble, M.(1983) Nature 303, 390–396.
Rand, J. H., Wu, X. X., Potter, B. J., Uson, R. R.& Gordon, R. E.(1993) Am J Pathol 142, 843–850.
Redwine, J. M., Blinder, K. L.& Armstrong, R. C.(1997) J Neurosci Res 50, 229–237.
Reisfeld, R. A., Harper, J. R.& Bumol, T. F.(1984) Crit Rev Immunol 5, 27–53.
Reynolds, R., Cenci Di Bello, I., Dawson, M.& Levine, J.(2001) Prog Brain Res 132, 165–174.
Reynolds, R.& Hardy, R.(1997) J Neurosci Res 47, 455–470.
Ross(1993) Nature 362, 801–809.
Rushing, E. J., Watson, M. L., Schold, S. C., Land, K. J.& Kokkinakis, D. M.(1998) J Neuropathol Exp Neurol 57, 1053–1060.
Rutka, J. T., Apodaca, G., Stern, R.& Rosenblum, M.(1988) J Neurosurg 69, 155–170.
Schiffer D., Cavalla, P.& Pilkington G. J.(1998) Proliferative properties of malignant Brain Tumors in BrainTumor Invasion: Biological, Clinical & Therapeutic Considerations(edited by Mikkelsen, T., Bjerkvig, B., Laerum, O.-D.& Rosenblum, M. L.) pp. 161–184. John Wiley-Liss Inc. ISBN 0-471-15452-0.
Schlingemann, R. O., Rietveld, F. J., De Waal, R. M., Ferrone, S.& Ruiter, D. J.(1990) Am J Pathol 136, 1393–1405.
Schrappe, M., Klier, F. G., Spiro, R. C., Waltz, T. A., Reisfeld, R. A.& Gladson, C. L.(1991) Cancer Res 51, 4986–4993.
Schwartz, S. M., Heimark, R. L.& Majesky, M. W.(1990) Physiol Rev 70, 1177–1209.
Scolding, N. J., Rayner, P. J.& Compston, D. A.(1999) Neuroscience 89, 1–4.
Shee, W. L., Ong, W. Y.& Lim, T. M.(1998) Brain Res 799, 292–300.
Shen, W. C.& Ryser, H. J.(1981) Biochem Biophys Res Commun 102, 1048–1054.
Shoshan, Y., Nishiyama, A., Chang, A., Mork, S., Barnett, G. H., Cowell, J. K., Trapp, B. D.& Staugaitis, S. M.(1999) Proc Natl Acad Sci USA 96, 10361–10366.
Silbergeld, D. L.& Chicoine, M. R.(1997) J Neurosurg 86, 525–531.
Sims, D., Horne, M. M., Creighan, M.& Donald, A.(1994) Anat Histol Embryol 23, 232–238.
Sims, D. E.(1986) Tissue Cell 18, 153–174.
Small, R. K., Riddle, P.& Noble, M.(1987) Nature 328, 155–157.
Smith, F. O., Rauch, C., Williams, D. E., March, C. J., Arthur, D., Hilden, J., Lampkin, B. C., Buckley, J. D., Buckley, C. V., Woods, W. G., Dinndorf, P. A., Sorensen, P., Kersey, J., Hammond, D.& Bernstein, I. D.(1996) Blood 87, 1123–1133.
Speiser, P., Gittelsohn, A. M.& Patz, A.(1968) Arch Ophthalmol 80, 332–337.
Stallcup, W. B., Dahlin, K.& Healy, P.(1990) J Cell Biol 111, 3177–3188.
Stallcup, W. B.& Dahlin-Huppe, K.(2001) J Cell Sci 114, 2315–2325.
Streit, W. J.& Kreutzberg, G. W.(1987) J Neurocytol 16, 249–260.
Sugimoto, Y., Taniguchi, M., Yagi, T., Akagi, Y., Nojyo, Y.& Tamamaki, N.(2001) Development 128, 3321–3330.
Sung, C. C., Collins, R., Li, J., Pearl, D. K., Coons, S. W., Scheithauer, B. W., Johnson, P. C.& Yates, A. J.(1996) Glycoconj J 13, 433–443.
Tanaka, K., Nogawa, S., Ito, D., Suzuki, S., Dembo, T., Kosakai, A.& Fukuuchi, Y.(2001) Neuroreport 12, 2169–2174.
Tillet, E., Ruggiero, F., Nishiyama, A.& Stallcup, W. B.(1997) J Biol Chem 272, 10769–10776.
Tilton, R. G., Kilo, C.& Williamson, J. R.(1979) Microvasc Res 18, 325–335.
Wahl, S. M., Hunt, D. A., Wakefield, L. M., McCartney-Francis, N., Wahl, L. M., Roberts, A. B.& Sporn, M. B.(1987) Proc Natl Acad Sci USA 84, 5788–5792.
Wilson, S. S., Baetge, E. E.& Stallcup, W. B.(1981) Dev Biol 83, 146–153.
Wolswijk, G.& Noble, M.(1989) Development 105, 387–400.
Wolswijk, G., Riddle, P. N.& Noble, M.(1990) Development 109, 691–698.
Wren, D., Wolswijk, G.& Noble, M.(1992) J Cell Biol 116, 167–176.
Yamamoto, M.& Yamamoto, K.(1994) Exp Cell Res 212, 62–68.
Yang, H. M.& Reisfeld, R. A.(1988a) Proc Natl Acad Sci USA 85, 1189–1193.
Yang, H. M.& Reisfeld, R. A.(1988b) J Natl Cancer Inst 80, 1154–1159.
Yanofsky, S. D., Baldwin, D. N., Butler, J. H., Holden, F. R., Jacobs, J. W., Balasubramanian, P., Chinn, J. P., Cwirla, S. E., Peters-Buhatt, E., Whitehorn, E. A., Tate, E. H., Akeson, A., Bowlin, T. L., Dower, W. J.& Barrett, R. W.(1996) Proc Natl Acad Sci USA 93, 7381–7386.
Zalutsky, M. R., Moseley, R. P., Benjamin, J. C., Colapinto, E. V., Fuller, G. N., Coakham, H. P.& Bigner, D. D.(1990) Cancer Res 50, 4105–4110.
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Chekenya, M., Pilkington, G.J. NG2 precursor cells in neoplasia: Functional, histogenesis and therapeutic implications for malignant brain tumours. J Neurocytol 31, 507 ppl=–521 (2002). https://doi.org/10.1023/A:1025795715377
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DOI: https://doi.org/10.1023/A:1025795715377