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NG2 precursor cells in neoplasia: Functional, histogenesis and therapeutic implications for malignant brain tumours

  • Published:
Journal of Neurocytology

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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References

  • 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.

    Google Scholar 

  • Arnett, H. A., Mason, J., Marino, M., Suzuki, K.& Matsushima, G. K.(2001) Nat Neurosci 4(11), 1116–1122.

    Google Scholar 

  • Ting, J. P. Ashley, D. M., Batra, S. K.& Bigner, D. D.(1997) J Neurooncol 35, 259–273.

    Google Scholar 

  • Back, S. A., Luo, N. L., Borenstein, N. S., Levine, J. M., Volpe, J. J.& Kinney, H. C.(2001) J Neurosci 21, 1302–1312.

    Google Scholar 

  • Balabanov, R.& Dore-Duffy, P.(1998) J Neurosci Res 53, 637–644.

    Google Scholar 

  • Barnett, S. C., Robertson, L., Graham, D., Allan, D.& Rampling, R.(1998) Carcinogenesis 19, 1529–1537.

    Google Scholar 

  • Barron, K. D.(1995) J Neuro Sci 134, 57–68.

    Google Scholar 

  • Behm, F. G., Smith, F. O., Raimondi, S. C., Pui, C. H.& Bernstein, I. D.(1996) Blood 87, 1134–1139.

    Google Scholar 

  • Behnke, J., Mach, J. P., Buchegger, F., Carrel, S., Delaloye, B.& De Tribolet, N.(1988) Br J Neurosurg 2, 193–197.

    Google Scholar 

  • Berens, M. E.& Giese A.(1999) Neoplasia 1, 208–219.

    Google Scholar 

  • 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.

    Google Scholar 

  • Bodmer, S., Strommer, K., Frei, K., Siepl, C., De Tribolet, N., Heid, I.& Fontana, A.(1989) J Immunol 143, 3222–3229.

    Google Scholar 

  • Boehm, T., Folkman, J., Browder, T.& O'Reilly, M. S.(1997) Nature 390, 404–407.

    Google Scholar 

  • Bolteus, A. J., Berens, M. E.& Pilkington, G. J.(2001) Curr Neurol Neurosci Rep 1, 225–232.

    Google Scholar 

  • Bu, J., Akhtar, N.& Nishiyama, A.(2001) Glia 34, 296–310.

    Google Scholar 

  • Buchegger, F., Mach, J. P., Leonnard, P.& Carrel, S.(1986) Cancer 58, 655–662.

    Google Scholar 

  • Bumol, T. F.& Reisfeld, R. A.(1982) Proc Natl Acad Sci USA 79, 1245–1249.

    Google Scholar 

  • Bumol, T. F., Walker, L. E.& Reisfeld, R. A.(1984) J Biol Chem 259, 12733–12741.

    Google Scholar 

  • Bumol, T. F., Wang, Q. C., Reisfeld, R. A.& Kaplan, N. O.(1983) Proc Natl Acad Sci USA 80, 529–533.

    Google Scholar 

  • Burg, M. A., Grako, K. A.& Stallcup, W. B.(1998) J Cell Physiol 177, 299–312.

    Google Scholar 

  • Burg, M. A., Nishiyama, A.& Stallcup, W. B.(1997) Exp Cell Res 235, 254–264.

    Google Scholar 

  • Burg, M. A., Pasqualini, R., Arap, W., Ruoslahti, E.& Stallcup, W. B.(1999) Cancer Res 59, 2869–2874.

    Google Scholar 

  • Burg, M. A., Tillet, E., Timpl, R.& Stallcup, W. B.(1996) J Biol Chem 271, 26110–26116.

    Google Scholar 

  • Burrows, F. J.& Thorpe, P. E.(1993) Proc Natl Acad Sci USA 90, 8996–9000.

    Google Scholar 

  • Butt, A. M., Duncan, A., Hornby, M. F., Kirvell, S. L., Hunter, A., Levine, J. M.& Berry, M.(1999) Glia 26, 84–91.

    Google Scholar 

  • Carrel, S., Accolla, R. S., Carmagnola, A. L.& Mach, J. P.(1980) Cancer Res 40, 2523–2528.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Chintala, S. K., Sawaya, R., Gokaslan, Z. L., Fuller, G.& Rao, J. S.(1996) Cancer Lett 101, 107–114.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • CUSHING (1928) Tumors Arising from the Blood-Vessels of the Brain: Angiomatous Malformations and Hemangioblastomas. Illanois: Spring-Field.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Diener, E., Diner, U. E., Sinha, A., Xie, S.& Vergidis, R.(1986) Science 231, 148–150.

    Google Scholar 

  • Doane, K. J., Howell, S. J.& Birk, D. E.(1998) Invest Ophthalmol Vis Sci 39, 263–275.

    Google Scholar 

  • Doetsch, F., Garcia-Verdugo, J. M.& Alvarezbuylla, A.(1999) Proc Natl Acad Sci USA 96, 11619–11624.

    Google Scholar 

  • Dou, C. L.& Levine, J. M.(1994) J Neurosci 14, 7616–7628.

    Google Scholar 

  • East, J. A., Mitchell, S. D.& Hart, I. R.(1993) Melanoma Res 3, 341–346.

    Google Scholar 

  • Edgar, D., Timpl, R.& Thoenen, H.(1984) Embo J 3, 1463–1468.

    Google Scholar 

  • Epenetos, A. A., Snook, D., Durbin, H., Johnson, P. M.& Taylor-Papadimitriou, J.(1986) Cancer Res 46, 3183–3191.

    Google Scholar 

  • Epenetos, A. A., Snook, D., Hooker, G., Lavender, J. P.& Halnan, K. E.(1984) Lancet 2, 169.

    Google Scholar 

  • 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.

    Google Scholar 

  • Fang, X., Burg, M. A., Barritt, D., Dahlinhuppe, K., Nishiyama, A.& Stallcup, W. B.(1999) Mol Biol Cell 10, 3373–3387.

    Google Scholar 

  • Fawcett, J. W.& Asher, R. A.(1999) Brain Res Bull 49, 377–391.

    Google Scholar 

  • Ferns, G. A., Raines, E. W., Sprugel, K. H., Motani, A. S., Reidy, M. A.& Ross, R.(1991) Science 253, 1129–1132.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Folkman, J.(1971) N Engl J Med 285, 1182–1186.

    Google Scholar 

  • Folkman, J.(1995) Nat Med 1, 27–31.

    Google Scholar 

  • Folkman, J., Watson, K., Ingber, D.& Hanahan, D.(1989) Nature 339, 58–61.

    Google Scholar 

  • Frisen, J., Johansson, C. B., Lothian, C.& Lendahl, U.(1998) Cell Mol Life Sci 54, 935–945.

    Google Scholar 

  • Fulton, B. P., Burne, J. F.& Raff, M. C.(1992) J Neurosci 12, 4816–4833.

    Google Scholar 

  • Gage, F. H.(1998) Curr Opin Neurobiol 8, 671–676.

    Google Scholar 

  • Garrigues, H. J., Lark, M. W., Lara, S., Hellstrom, I., Hellstrom, K. E.& Wight, T. N.(1986) J Cell Biol 103, 1699–1710.

    Google Scholar 

  • Giese, A., Loo, M. A., Tran, N., Haskett, D., Coons, S. W.& Berens, M. E.(1996) Int J Cancer, 67, 275–282.

    Google Scholar 

  • Gehrmann, J., Matsumoto, Y.& Kreutzberg, G. W.(1995) Brain Res Brain Res Rev 20, 269–287.

    Google Scholar 

  • Giordana, M. T., Germano, I., Giaccone, G., Mauro, A., Migheli, A.& Schiffer, D.(1985) Acta Neuropathol (Berl) 67, 51–57.

    Google Scholar 

  • Gladson, C. L.(1999) J Neuropathol Exp Neurol 58, 1029–1040.

    Google Scholar 

  • Goldman, J. E.(2000) J Neurosci Res 59, 410–412.

    Google Scholar 

  • Goodson, R. J., Doyle, M. V., Kaufman, S. E.& Rosenberg, S.(1994) Proc Natl Acad Sci USA 91, 7129–7133.

    Google Scholar 

  • Goretzki, L., Burg, M. A., Grako, K. A.& Stallcup, W. B.(1999) J Biol Chem 274, 16831–16837.

    Google Scholar 

  • Goretzki, L., Lombardo, C. R.& Stallcup, W. B.(2000) J Biol Chem 275, 28625–28633.

    Google Scholar 

  • Gould, E., Reeves, A. J., Graziano, M. S.& Gross, C. G.(1999) Science 286, 548–552.

    Google Scholar 

  • Gould, E., Tanapat, P., McEwen, B. S., Flugge, G.& Fuchs, E.(1998) Proc Natl Acad Sci USA 95, 3168–3171.

    Google Scholar 

  • Grako, K. A., Ochiya, T., Barritt, D., Nishiyama, A.& Stallcup, W. B.(1999) J Cell Sci 112(Pt 6), 905–915.

    Google Scholar 

  • Grako, K. A.& Stallcup, W. B.(1995) Exp Cell Res 221, 231–240.

    Google Scholar 

  • Gratsa, A., Rooprai, H. K., Rogers, J. P., Martin, K. K.& Pilkington, G. J.(1997) Anticancer Res 17, 4111–4117.

    Google Scholar 

  • Hall, A., Giese, N. A.& Richardson, W. D.(1996) Development 122, 4085–4094.

    Google Scholar 

  • Hanahan, D., Christofori, G., Naik, P.& Arbeit, J.(1996) Eur J Cancer 32A, 2386–2393.

    Google Scholar 

  • Harper, J. R., Bumol, T. F.& Reisfeld, R. A.(1984) J Immunol 132, 2096–2104.

    Google Scholar 

  • Harper, J. R.& Reisfeld, R. A.(1983) J Natl Cancer Inst 71, 259–263.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hirschi, K. K.& D'amore, P. A.(1997) Exs 79, 419–428.

    Google Scholar 

  • Humphries, M. J.(2000) Trends Pharmacol Sci 21, 29–32.

    Google Scholar 

  • Hwang, K. M., Fodstad, O., Oldham, R. K.& Morgan, A. C. Jr.(1985) Cancer Res 45, 4150–4155.

    Google Scholar 

  • Iida, J., Meijne, A. M., Spiro, R. C., Roos, E., Furcht, L. T.& McCarthy, J. B.(1995) Cancer Res 55, 2177–2185.

    Google Scholar 

  • Ito, D., Imai, Y., Ohsawa, K., Nakajima, K., Fukuuchi, Y.& Kohsaka, S.(1998) Brain Res Mol Brain Res 57, 1–9.

    Google Scholar 

  • Jain, R. K.& Baxter, L. T.(1988) Cancer Res 48, 7022–7032.

    Google Scholar 

  • Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U.& Frisen, J.(1999) Cell 96, 25–34.

    Google Scholar 

  • Jones, L. L., Yamaguchi, Y., Stallcup, W. B.& Tuszynski, M. H.(2002) J Neurosci 22, 2792–2803.

    Google Scholar 

  • Kerbel, R. S.(1991) Bioessays 13, 31–36.

    Google Scholar 

  • Kerbel, R. S.(1997) Nature 390, 335–336.

    Google Scholar 

  • Kleihues, P., Burger, P. C.& Scheithauer, B. W.(1993) Brain Pathol 3, 255–268.

    Google Scholar 

  • Kleihues, P.& Cavenee. W.(2000) World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of the Nervous System. Lyon: Oxford University Press.

    Google Scholar 

  • Kligman, D.& Hilt, D. C.(1988) Trends Biochem Sci 13, 437–443.

    Google Scholar 

  • 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.

    Google Scholar 

  • Koivunen, E., Restel, B. H., Rajotte, D., Lahdenranta, J., Hagedorn, M., Arap, W.& Pasqualini, R.(1999b) Methods Mol Biol 129, 3–17.

    Google Scholar 

  • Koivunen, E., Wang, B.& Ruoslahti, E.(1995) Biotechnology (NY) 13, 265–270.

    Google Scholar 

  • 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.

    Google Scholar 

  • Koochekpour, S.& Pilkington, G. J.(1996) Cancer Lett 104, 97–102.

    Google Scholar 

  • Kuo, H. J., Maslen, C. L., Keene, D. R.& Glanville, R. W.(1997) J Biol Chem 272, 26522–26529.

    Google Scholar 

  • Kuppner, M. C., Van Meir, E., Gauthier, T., Hamou, M. F.& De Tribolet, N.(1992) Int J Cancer 50, 572–577.

    Google Scholar 

  • Larsen, R. H., Akabani, G., Welsh, P.& Zalutsky, M. R.(1998) Radiat Res 149, 155–162.

    Google Scholar 

  • Leger, O., Johnson-Leger, C., Jackson, E., Coles, B.& Dean, C.(1994) Int J Cancer 58, 700–705.

    Google Scholar 

  • Lemmon, V., Farr, K. L.& Lagenaur, C.(1989) Neuron 2, 1597–1603.

    Google Scholar 

  • Leong, S. K.& Ling, E. A.(1992) Glia 6, 39–47.

    Google Scholar 

  • Levine, J. M.(1994) J Neurosci 14, 4716–4730.

    Google Scholar 

  • Levine, J. M.& Card, J. P.(1987) J Neurosci 7, 2711–2720.

    Google Scholar 

  • Levine, J. M., Enquist, L. W.& Card, J. P.(1998) Glia 23, 316–328.

    Google Scholar 

  • Levine, J. M., Reynolds, R.& Fawcett, J. W.(2001) Trends Neurosci 24, 39–47.

    Google Scholar 

  • Levine, J. M., Stincone, F.& Lee, Y. S.(1993) Glia 7, 307–321.

    Google Scholar 

  • Levison, S. W., Young, G. M.& Goldman, J. E.(1999) J Neurosci Res 57, 435–446.

    Google Scholar 

  • Lin, X. H., Dahlin-Huppe, K.& Stallcup, W. B.(1996) J Cell Biochem 63, 463–477.

    Google Scholar 

  • Lindahl, P.& Betsholtz, C.(1998) Curr Opin Nephrol Hypertens 7, 21–26.

    Google Scholar 

  • Lindahl, P., Johansson, B. R., Leveen, P.& Betsholtz, C.(1997) Science 277, 242–245.

    Google Scholar 

  • Lindmo, T., Boven, E., Cuttitta, F., Fedorko, J.& Bunn, P. A. Jr.(1984) J Immunol Methods 72, 77–89.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • McKnight, A. J., Macfarlane, A. J., Dri, P., Turley, L., Willis, A. C.& Gordon, S.(1996) J Biol Chem 271, 486–489.

    Google Scholar 

  • McTigue, D. M., Wei, P.& Stokes, B. T.(2001) J Neurosci 21, 3392–3400.

    Google Scholar 

  • Merzak, A., Koocheckpour, S.& Pilkington, G. J.(1994) Cancer Res 54, 3988–3992.

    Google Scholar 

  • Merzak, A., Koochekpour, S., McCrea, S., Roxanis, Y.& Pilkington, G. J.(1995) Mol Chem Neuropathol 24, 121–135.

    Google Scholar 

  • Midwood, K. S.& Salter, D. M.(2001) J Pathol 195, 631–635.

    Google Scholar 

  • Miller, B., Sheppard, A. M., Bicknese, A. R.& Pearlman, A. L.(1995) J Comp Neurol 355, 615–628.

    Google Scholar 

  • Morgan, A. C., Jr., Galloway, D. R.& Reisfeld, R. A.(1981) Hybridoma 1, 27–36.

    Google Scholar 

  • Murayama, O., Nishida, H.& Sekiguchi, K.(1996) J Biochem (Tokyo) 120, 445–451.

    Google Scholar 

  • 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.

    Google Scholar 

  • Nishiyama, A.(2001) Hum Cell 14, 77–82.

    Google Scholar 

  • Nishiyama, A., Dahlin, K. J., Prince, J. T., Johnstone, S. R.& Stallcup, W. B.(1991) J Cell Biol 114, 359–371.

    Google Scholar 

  • Nishiyama, A., Lin, X. H., Giese, N., Heldin, C. H.& Stallcup, W. B.(1996a) J Neurosci Res 43, 299–314.

    Google Scholar 

  • Nishiyama, A., Lin, X. H., Giese, N., Heldin, C. H.& Stallcup, W. B.(1996b) J Neurosci Res 43, 315–330.

    Google Scholar 

  • Nishiyama, A.& Stallcup, W. B.(1993) Mol Biol Cell 4, 1097–1108.

    Google Scholar 

  • Nishiyama, A., Yu, M., Drazba, J. A.& Tuohy, V. K.(1997) J Neurosci Res 48, 299–312.

    Google Scholar 

  • 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.

    Google Scholar 

  • Noble, A. M.-P.(2001) Glial Restricted Precursors. Totowa, New Jersey: Humana Press.

    Google Scholar 

  • Noble, M., Murray, K., Stroobant, P., Waterfield, M. D.& Riddle, P.(1988) Nature 333, 560–562.

    Google Scholar 

  • Orlidge, A.& D'amore, P. A.(1987) J Cell Biol 105, 1455–1462.

    Google Scholar 

  • Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E.& Stallcup, W. B.(2001) Dev Dyn 222, 218–227.

    Google Scholar 

  • Ozerdem, U., Monosov, E.& Stallcup, W. B.(2002) Microvasc Res 63, 129–134.

    Google Scholar 

  • Palmer, T. D., Takahashi, J.& Gage, F. H.(1997) Mol Cell Neurosci 8, 389–404.

    Google Scholar 

  • Paulus, W., Roggendorf, W.& Schuppan, D.(1988) Virchows Arch A Pathol Anat Histopathol 413, 325–332.

    Google Scholar 

  • Pedersen, P. H., Marienhagen, K., Mork, S.& Bjerkvig, R.(1993) Cancer Res 53, 5158–5165.

    Google Scholar 

  • Pennington, M. E., Lam, K. S.& Cress, A. E.(1996) Mol Divers 2, 19–28.

    Google Scholar 

  • Pilkington, G. J.(1994) Brain Pathology 4, 157–166.

    Google Scholar 

  • Pilkington, G. J.(1996) Brazilian Journal of Medical and Biological Research 29, 1159–1172.

    Google Scholar 

  • Pilkington, G. J.(1992) Neuropathol Appl Neurobiol 18, 434–442.

    Google Scholar 

  • Pilkington, G. J., Dunan, J. R., Rogers, J. P., Clarke, T. M.& Knott, J. C.(1993) Neurosci Lett 149, 1–5.

    Google Scholar 

  • Pouly, S., Becher, B., Blain, M.& Antel, J. P.(1999) Glia 27, 259–268.

    Google Scholar 

  • Pouly, S., Prat, A., Blain, M., Olivier, A.& Antel, J.(2001) Acta Neuropathol (Berl) 102, 313–320.

    Google Scholar 

  • Raff, M. C., Miller, R. H.& Noble, M.(1983) Nature 303, 390–396.

    Google Scholar 

  • Rand, J. H., Wu, X. X., Potter, B. J., Uson, R. R.& Gordon, R. E.(1993) Am J Pathol 142, 843–850.

    Google Scholar 

  • Redwine, J. M., Blinder, K. L.& Armstrong, R. C.(1997) J Neurosci Res 50, 229–237.

    Google Scholar 

  • Reisfeld, R. A., Harper, J. R.& Bumol, T. F.(1984) Crit Rev Immunol 5, 27–53.

    Google Scholar 

  • Reynolds, R., Cenci Di Bello, I., Dawson, M.& Levine, J.(2001) Prog Brain Res 132, 165–174.

    Google Scholar 

  • Reynolds, R.& Hardy, R.(1997) J Neurosci Res 47, 455–470.

    Google Scholar 

  • Ross(1993) Nature 362, 801–809.

    Google Scholar 

  • Rushing, E. J., Watson, M. L., Schold, S. C., Land, K. J.& Kokkinakis, D. M.(1998) J Neuropathol Exp Neurol 57, 1053–1060.

    Google Scholar 

  • Rutka, J. T., Apodaca, G., Stern, R.& Rosenblum, M.(1988) J Neurosurg 69, 155–170.

    Google Scholar 

  • 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.

    Google Scholar 

  • Schrappe, M., Klier, F. G., Spiro, R. C., Waltz, T. A., Reisfeld, R. A.& Gladson, C. L.(1991) Cancer Res 51, 4986–4993.

    Google Scholar 

  • Schwartz, S. M., Heimark, R. L.& Majesky, M. W.(1990) Physiol Rev 70, 1177–1209.

    Google Scholar 

  • Scolding, N. J., Rayner, P. J.& Compston, D. A.(1999) Neuroscience 89, 1–4.

    Google Scholar 

  • Shee, W. L., Ong, W. Y.& Lim, T. M.(1998) Brain Res 799, 292–300.

    Google Scholar 

  • Shen, W. C.& Ryser, H. J.(1981) Biochem Biophys Res Commun 102, 1048–1054.

    Google Scholar 

  • 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.

    Google Scholar 

  • Silbergeld, D. L.& Chicoine, M. R.(1997) J Neurosurg 86, 525–531.

    Google Scholar 

  • Sims, D., Horne, M. M., Creighan, M.& Donald, A.(1994) Anat Histol Embryol 23, 232–238.

    Google Scholar 

  • Sims, D. E.(1986) Tissue Cell 18, 153–174.

    Google Scholar 

  • Small, R. K., Riddle, P.& Noble, M.(1987) Nature 328, 155–157.

    Google Scholar 

  • 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.

    Google Scholar 

  • Speiser, P., Gittelsohn, A. M.& Patz, A.(1968) Arch Ophthalmol 80, 332–337.

    Google Scholar 

  • Stallcup, W. B., Dahlin, K.& Healy, P.(1990) J Cell Biol 111, 3177–3188.

    Google Scholar 

  • Stallcup, W. B.& Dahlin-Huppe, K.(2001) J Cell Sci 114, 2315–2325.

    Google Scholar 

  • Streit, W. J.& Kreutzberg, G. W.(1987) J Neurocytol 16, 249–260.

    Google Scholar 

  • Sugimoto, Y., Taniguchi, M., Yagi, T., Akagi, Y., Nojyo, Y.& Tamamaki, N.(2001) Development 128, 3321–3330.

    Google Scholar 

  • 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.

    Google Scholar 

  • Tanaka, K., Nogawa, S., Ito, D., Suzuki, S., Dembo, T., Kosakai, A.& Fukuuchi, Y.(2001) Neuroreport 12, 2169–2174.

    Google Scholar 

  • Tillet, E., Ruggiero, F., Nishiyama, A.& Stallcup, W. B.(1997) J Biol Chem 272, 10769–10776.

    Google Scholar 

  • Tilton, R. G., Kilo, C.& Williamson, J. R.(1979) Microvasc Res 18, 325–335.

    Google Scholar 

  • 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.

    Google Scholar 

  • Wilson, S. S., Baetge, E. E.& Stallcup, W. B.(1981) Dev Biol 83, 146–153.

    Google Scholar 

  • Wolswijk, G.& Noble, M.(1989) Development 105, 387–400.

    Google Scholar 

  • Wolswijk, G., Riddle, P. N.& Noble, M.(1990) Development 109, 691–698.

    Google Scholar 

  • Wren, D., Wolswijk, G.& Noble, M.(1992) J Cell Biol 116, 167–176.

    Google Scholar 

  • Yamamoto, M.& Yamamoto, K.(1994) Exp Cell Res 212, 62–68.

    Google Scholar 

  • Yang, H. M.& Reisfeld, R. A.(1988a) Proc Natl Acad Sci USA 85, 1189–1193.

    Google Scholar 

  • Yang, H. M.& Reisfeld, R. A.(1988b) J Natl Cancer Inst 80, 1154–1159.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

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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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